Next Article in Journal
Assessment of the Impact of Small-Scale Irrigation on Household Livelihood Improvement at Gubalafto District, North Wollo, Ethiopia
Next Article in Special Issue
Crop Management as an Agricultural Adaptation to Climate Change in Early Modern Era: A Comparative Study of Eastern and Western Europe
Previous Article in Journal
Phosphorus Bioavailability: A Key Aspect for Conserving this Critical Animal Feed Resource with Reference to Broiler Nutrition
Previous Article in Special Issue
Small Scale Farmers’ Indigenous Agricultural Adaptation Options in the Face of Declining or Stagnant Crop Yields in the Fako and Meme Divisions of Cameroon
Article Menu

Export Article

Agriculture 2016, 6(2), 26; doi:10.3390/agriculture6020026

Review
Selection and Breeding of Suitable Crop Genotypes for Drought and Heat Periods in a Changing Climate: Which Morphological and Physiological Properties Should Be Considered?
Lyudmila Simova-Stoilova 1, Valya Vassileva 1 and Urs Feller 2,*
1
Institute of Plant Physiology and Genetics, Bulgarian Academy of Sciences, Acad. G. Bonchev Street, Bldg. 21, 1113 Sofia, Bulgaria
2
Institute of Plant Sciences and Oeschger Center for Climate Change Research (OCCR), University of Bern, Altenbergrain 21, CH-3013 Bern, Switzerland
*
Correspondence: Tel.: +41-31-302-2109
Academic Editor: Annelie Holzkämper
Received: 19 April 2016 / Accepted: 25 May 2016 / Published: 1 June 2016

Abstract

:
Selection and breeding of genotypes with improved drought/heat tolerance become key issues in the course of global change with predicted increased frequency of droughts or heat waves. Several morphological and physiological plant traits must be considered. Rooting depth, root branching, nutrient acquisition, mycorrhization, nodulation in legumes and the release of nutrients, assimilates or phytohormones to the shoot are relevant in root systems. Xylem embolism and its repair after a drought, development of axillary buds and solute channeling via xylem (acropetal) and phloem (basipetal and acropetal) are key processes in the stem. The photosynthetically active biomass depends on leaf expansion and senescence. Cuticle thickness and properties, epicuticular waxes, stomatal regulation including responses to phytohormones, stomatal plugs and mesophyll resistance are involved in optimizing leaf water relations. Aquaporins, dehydrins, enzymes involved in the metabolism of compatible solutes (e.g., proline) and Rubisco activase are examples for proteins involved in heat or drought susceptibility. Assimilate redistribution from leaves to maturing fruits via the phloem influences yield quantity and quality. Proteomic analyses allow a deeper insight into the network of stress responses and may serve as a basis to identify suitable genotypes, although improved stress tolerance will have its price (often lowered productivity under optimal conditions).
Keywords:
drought; heat; climate change; crop genotypes; morphology; physiology; stress susceptibility; assimilate allocation; yield

1. Introduction

Besides increasing atmospheric CO2 concentration and higher average temperature, more frequent and/or more severe extreme climatic events including extended drought periods and superimposed heat waves as predicted by climate change models represent challenges for agriculture during the next decades [1,2,3,4]. Selection and breeding of suitable crop genotypes are key aspects in this context [5,6]. How should these genotypes behave? The superficial answer would be that they should be less susceptible to abiotic stresses, but a closer and critical look on specific functions and interactions on the whole plant level may help to evaluate the sustainable performance of crop species and varieties in a more comprehensive manner [6,7,8]. The overall performance of a species or a variety depends on the plant integral activity during the pre-stress phase, the stress period(s) and the recovery phase(s) [9]. Key aspects for the comparison of drought sensitivity in crop varieties are summarized in Figure 1.
Performance during non-stress phases is often lower for drought-tolerant than for well yielding standard varieties (Figure 1A) [10]. The performance during moderate drought may decline more rapidly and then remain stable on a lower level in drought-tolerant genotypes, while standard varieties may decline more steadily (Figure 1B). The down-regulation of physiological activities in stress-tolerant varieties may improve the chances to survive, save resources (e.g., water during drought stress) and serve as a basis for rapid recovery after the stress phase [9]. On the other hand, less drought-tolerant varieties may be initially more productive during the stress period, but may then be more severely damaged and recovering less well than a more tolerant variety [9]. An important point is the velocity and degree of recovery after the stress period (Figure 1C). The low activity level reached after a severe drought (Figure 1D), the time course for physiological activities during a subsequent recovery phase (Figure 1E) and the completeness of recovery (Figure 1F) are important for genotype comparisons [11,12].
Another aspect to be considered is that good overall performance of crop plants under stress does not necessarily coincide with yield stability [10]. Breeding for stress-tolerant crops should focus on acceptable yields under limited environmental conditions and not only on survival after stress [8]. Besides, combined response to drought and heat, which often co-occur or superimpose, could differ from adaptation to individual stresses [13,14,15]. For example, proline is accumulated under drought, but not under water stress combined with high temperature; strong activation of starch breakdown and malate metabolism in support to the mitochondrial respiration is typical for the combination of drought and heat but not for these stresses applied separately [14,15].
Several recent reviews have summarized the current knowledge of plant response to drought and high temperature stresses at morphological, physiological and phenological levels [16,17,18,19,20,21]. The aim of this review is to identify morphological and physiological properties that are important for drought and/or heat tolerance in crop plants and for sustainable crop production. Such key properties serve as a basis for the selection of suitable crops or genotypes on one hand and for breeding new varieties to be grown in a changing climate on the other hand. Special attention is paid on the search for suitable molecular markers for assisted selection and breeding, including some protein markers.

2. Root Morphology and Physiology

Heat waves affect directly the shoot, while roots, being in direct contact with the drying soil, are the first organs that suffer from, sense and respond to drought stress, transmitting the stress signal to the whole plant. The water potential in the soil declines during a drought period, but there may be considerable differences in the vertical (depth) and in the horizontal (patchiness) direction (Figure 2) [22,23,24]. Since strong vertical gradients for soil water potential are very likely, rooting depth must be a key parameter (Figure 2A) [25,26,27]. However, from a comprehensive study including more than 40 species it became evident that rooting depth is not equally plastic [28]. Rooting depth in the majority of these species was not significantly affected by soil drying, while in seven species it was increased and in five species even decreased in drying soil [28]. These findings indicate that caution is recommended when generalizing such results and that the different response may be relevant for species competition (e.g., in grasslands). It must be borne in mind that, depending on the actual weather during a drought period, minor quantities of water may be available in the top soil layer as a consequence of minor precipitation(s) or of dew condensation, while the water content in lower soil layers may not be improved by these events. Soil temperature near the surface depends on many factors (e.g., photon flux density, leaf area index, soil color, surface structure, air convection), which may influence heating by solar irradiation and heat dissipation. Therefore, interactions between various factors influence soil water availability as well as soil temperature pattern and finally influence the development of crop roots in a complex manner [29,30,31,32].
Root architecture depends on root branching as well as on the length of the various roots (Figure 2B) and is relevant for the exploration of soil regions with accessible water during a drought period [29,30]. Besides species-specific differences between crop plants grown under non-stress conditions, the plasticity of the root system in response to changing environment should be considered when breeding for stress tolerance [31,32]. Root architecture is affected by the soil water, temperature and nutrients, and additionally by soil microbial communities and microbial-plant interactions [32,33,34,35,36,37]. A good correlation between reduced lateral root branching and drought tolerance has been reported for maize [30,35], but the “rooting depth paradigm” is questioned recently [38]. A smaller number of longer lateral roots are found in maize genotypes with a good drought tolerance [30]. Since root branching is influenced by the availability of nitrogen [30,39,40], of phosphorus [40,41] and other nutrients in the soil [42], a “conflict of interest” in the acquisition of water and mineral nutrients may become relevant (especially when water is available in lower soil layers and limiting nutrients are left after fertilizer application mainly in the top layers).
Besides root architecture, physiological activities in roots including nutrient uptake, assimilation and xylem loading [43,44,45,46], release of phytohormones to the shoot [47,48,49,50,51] as well as root storage functions respond to heat and drought [52,53,54,55,56] (Figure 2C,F,G). Root hydraulic conductivity is another important parameter in this context [53]. The supply of shoots with N, P and K (based on the uptake into the roots, xylem loading in the roots and acropetal transport in the xylem) was found to be negatively influenced by drought in maize [45,46]. Possible mechanisms include the competition for phloem-borne carbon skeletons between root growth, nutrient uptake/assimilation and the loading into the xylem with an increased overall solute concentration and a decreased transport velocity. Nitrate uptake in maize is decreased during a drought period, but may increase again during a subsequent recovery phase [43]. Besides the activities of newly formed roots, older roots may recover to some extent after the stress period [43]. Considerable differences in nitrogen use efficiency were detected in tomato plants subjected to drought indicating that this plasticity might be relevant for selecting or breeding genotypes which are less sensitive to soil drying [44]. For the acquisition of potassium and other ions under drought stress it is important to distinguish between ion uptake into cortical cells mediated by specific translocator proteins and the subsequent loading of the ions into the xylem in the stele of stressed roots [57,58,59,60]. The two processes are affected differently by osmotic stress, a fact which must be borne in mind when evaluating responses of crop plants to drought [57,58,59,60]. An increased production of abscisic acid in roots and the release of this phytohormone via the xylem to the shoot where it is involved in the regulation of stomatal opening has been reported for several plant species [47,49,50]. Jasmonic acid may stimulate the production of abscisic acid in drought-stressed roots [49]. Transgenic Agrostis stolonifera plants with increased cytokinin synthesis have been found to be more drought-tolerant than control plants [48]. In these experiments, expression of isopentenyl transferase under control of the senescence-inducible SAG12 promoter increased cytokinin contents in roots and leaves, which resulted in less pronounced drought-induced senescence, functionally longer metabolic processes (including photosynthesis, respiration, amino acid metabolism and detoxification of reactive oxygen species) and improved overall drought tolerance [48]. Therefore, modifications in cytokinin biosynthesis and signaling might be helpful for breeding more drought-tolerant crops. A down-regulation of ethylene biosynthesis was reported for Medicago truncatula under water deprivation [51]. From these findings it becomes evident that the whole hormonal network must be considered for the identification of genotypes performing well under drought stress. Carbohydrates and nitrogenous compounds in the roots of drought-stressed plants are important for drought survival and for the formation of new leaves and for physiological activities in the post-stress phase [13,52,53]. Vegetative storage proteins accumulating under drought in the taproot of alfalfa are identified as important players in the nitrogen dynamics in plants subjected to increased CO2 and abiotic stresses [53].
Mycorrhization is highly important for the acquisition of phosphorus and other mineral nutrients (Figure 2D) [56,61,62,63,64,65,66,67,68,69,70]. These interactions between higher plants and fungi are sensitive to abiotic stresses on one hand and influence plant stress responses on the other hand [56,61,63,64,65,66,67,68]. Favorable effects of mycorrhiza in drought stressed plants have been reported for a series of plant species [66,67,68,70]. Interactions of higher plant with mycorrhiza (as well as root hairs) are not only relevant for the well-known acquisition of mineral nutrients, but may also play an important role in water fluxes from a drying soil into crop plants [62,63,64,65,66,67,68,69,70].
Legume plants possess the unique ability to fix atmospheric nitrogen via a symbiotic relationship with soil bacteria belonging to the genera Rhizobium (Figure 2E) [71]. This ability naturally enhances the nitrogen content in soils and reduces the need for nitrogen fertilizers, which makes their cultivation a sustainable practice in soil fertility maintenance and organic farming [72]. The legumes, such as soybean, common bean, broad bean, pea, chickpea and cowpea are widely cultivated as a valuable nutrition source [73,74] or offer a large potential for sustainable biofuel production [75]. However, the symbiotic relationships are highly vulnerable to extreme environmental conditions [76]. Drought is one of the major adverse factors suppressing symbiotic nitrogen fixation [77]. Water deprivation negatively affects both symbiotic partners and all stages of the establishment and functioning of symbiotic systems [64,78,79]. Most rhizobial symbionts have reduced viability and mobility under drought [80,81]. However, compared to host legume plants, rhizobial bacteria are more resistant and resilient to soil drought [82]. Host root growth and root hairs that are associated with rhizobial infection [83] are inhibited under exposure to water deprivation, which lead to a decrease in the number of infection threads and inhibition of nodulation [84]. At the next stages of the symbiotic partnership, drought can inhibit development of nodules, and triggers frequently premature nodule senescence. In general, the drought-induced inhibition of the rate of symbiotic nitrogen fixation could be related to several main factors: reduced carbon flux from the host plant leading to low ATP content, decreased shoot nitrogen demand, lower xylem translocation rate due to a decreased transpiration rate, drought-induced changes in nodule oxygen permeability resulting in low oxygen levels, decreased metabolic enzyme activity, and nitrogen feedback inhibition [64,85,86]. The latter is more pronounced in tropical ureide-exporting legumes [87,88], whereas temperate amide exporting legumes are generally more tolerant to drought than the ureide exporters [89]. This could be mainly attributed to the accumulation of ureides in nodules and shoots of drought-stressed plants [78,90,91]. Water deprivation causes oxidative stress in legumes, which leads to an extensive nodule damage and decreased nitrogen fixation [92]. It has been suggested that nodules with an increased antioxidant defense can have a higher drought tolerance [93,94,95]. Therefore, the performance of symbiotic systems under drought is a multifactorial trait, and different components of symbiotic relationships must be considered when breeding legumes with improved abiotic stress tolerance.

3. Stem Properties and Solute Allocation via Xylem and Phloem

A major function of the stem in annual crops is the solute transport between the root system and the aerial parts (Figure 2H). Inorganic nutrients (e.g., nitrate, sulfate, phosphate, cations), assimilates (e.g., amino acids or ureides deriving from assimilatory processes in roots) and phytohormones (e.g., abscisic acid representing a root-to-shoot signal) are transported with the transpiration stream in the xylem to the aerial plant parts (preferentially to active leaves) [44,45,46,96]. Shabala et al. [96] nicely summarized in a recent review article the large series of drought effects on xylem sap composition and root-to-shoot signaling including chemical changes (e.g., compounds mentioned above), physical signals (e.g., electric or hydraulic effects) and waves (e.g., reactive oxygen species or calcium concentration) [96]. From these effects it became evident that the signals from drought-stressed roots to the shoot are complex and cannot be reduced to an altered concentration of one or two compounds [96]. Xylem embolism in drought-exposed plants and its repair are highly relevant for the transport of water and solutes from the roots to the various shoot parts [97,98,99]. Redistribution processes via the phloem are controlled by the source/sink network with leaves, roots and maturing fruits as major players. This network can be considerably disturbed by abiotic stresses [100,101,102,103]. Related to this transport functions is the capacity of stems and petioles to store solutes (especially carbohydrates and amino acids) [104,105]. An accumulation of solutes may be caused by the altered source/sink network under abiotic stress and may be important for a subsequent recovery phase [105]. From a study with isogenic lines of Sorghum bicolor subjected to abiotic stresses it became evident that stem reserves strongly influence grain filling [104]. Another important point during drought stress and recovery is the fate of the shoot apex (i.e., reversible or irreversible damages) [100]. New leaves may be formed from axillary buds of previously stressed plants, resulting in different plant architecture than unstressed plants [100].

4. Leaf Morphology and Physiology

The photosynthetic performance during heat and drought periods depends on morphological and physiological leaf properties as summarized in Figure 3 [100]. The thickness and the properties of the cuticle (Figure 3A) as well as the deposition of epicuticular waxes (Figure 3B) are relevant for the non-stomatal transpiration, while the regulation of stomatal opening (Figure 3C) and in some plants also the formation of a stomatal plug (Figure 3D) are key factors for the regulation of stomatal transpiration. CO2 availability for photosynthesis in the mesophyll (Figure 3G) depends on stomatal and non-stomatal conductance (Figure 3C–E) [106].
Water, nutrients and organic compounds including phytohormones (e.g., ABA) are transported from the roots to the leaves in the xylem (Figure 3F). Changes in these fluxes affect leaf morphology and functions in a complex manner and influence finally plant productivity and yield. Since heat and drought impacts on photosynthesis and leaf physiology were reviewed recently [6,7,100,103] these aspects are only briefly summarized here in Figure 3. Gas exchange between the atmosphere and the photosynthetically active mesophyll cells is a key aspect and depends on properties of the cuticle, stomatal conductance and mesophyll conductance [106]. Stomatal density and pore area (long-term adaptation, no longer influenced in fully expanded leaves) and the regulation of stomatal opening (reversible short-term adaptation) are highly important for the control of stomatal transpiration and water use efficiency in drought-stressed plants [107,108,109,110]. A reduced stomatal density in halophytes exposed to salt stress (compared to unstressed control plants) was reported by several groups [107,108,109,110] and such adaptations were also considered for selecting/breeding crop varieties with improved abiotic stress tolerance by “learning from halophytes” [109]. Besides the morphological adaptations in drought-exposed leaves, other important mechanisms are based on changes in the protein pattern (e.g., accumulation of chaperonins or increased activities of enzymes involved in the detoxification of reactive oxygen species or the production of compatible solutes [18,103]. Two aspects of abiotic stress impacts relevant for genotype selection and breeding are emphasized here and discussed in more detail: intactness of organelles (especially chloroplasts and mitochondria) and reactive oxygen species (production and detoxification).
Water shortage affects growth and development of crop plants at multiple levels of biological organization [111]. Depending on drought intensity, multiple abnormalities occur in cellular organelles and structures [112,113]. Under drought, the leaf mesophyll cells contain chloroplasts and mitochondria of irregular shape and size [114,115,116,117]. The chloroplast ultrastructure is compromised, manifested by swollen granal compartments, disrupted chloroplast membranes, accumulation of plastoglobuli and a reduced size/lack of starch grains [116,117]. Drought-affected mitochondria are mostly enlarged, often devoid of cristae, and possess large electron-transparent areas [116]. The damages on subcellular level, in part, depend on the level of drought tolerance of the crop genotypes. Leaf cell organelles in the drought-tolerant genotypes are better preserved, whereas the chloroplast and mitochondrial structure of the sensitive cultivars is severely disorganized, which leads to organelle dysfunction. All the visual structural alterations can be easily converted into very informative numerical data by a quantitative morphometric analysis [26,116,117]. Therefore, the intactness of subcellular structures could be considered as an additional trait, contributing to crop improvement and could serve as a reliable stress marker in the selection of sustainable crop genotypes.
Production of short-lived activated oxygen (ROS—reactive oxygen species: singlet oxygen, superoxide anion, hydroperoxide radical, hydrogen peroxide, hydroxyl radical) and keeping them at safe local steady state level is indispensable for normal metabolic processes in every plant tissue [118,119,120]. Major sources of ROS are the electron transport chains in chloroplasts and mitochondria and photorespiration in peroxisomes; local active production and utilization of ROS also occurs in the apoplast [120]. The steady state level of ROS usually corresponds to tissue metabolic activity, depends on the subcellular compartment, and normally is strictly controlled over space and time. Plants possess double enzymatic and non-enzymatic ROS scavenging systems, represented by several protective enzymes: superoxide dismutases, catalases, various peroxidases including unspecific, ascorbate and glutathione peroxidases, glutathione reductase and others, as well as by low-molecular metabolites among which the most important are ascorbic acid, glutathione, carotenoids, tocopherols [118,119,120]. These systems successfully cooperate, for example in the ascorbate—glutathione cycle which is key ROS detoxifying system in the cytosol and organelles.
Many environmental constraints lead to disbalance in metabolism and overproduction of ROS. The early transient increase of ROS serves as a signal for an unfavorable change [119,120,121]. Prolonged or/and severe abiotic stress leads to development of secondary oxidative stress and mobilization of the enzymatic and non-enzymatic defense systems as shown in Table 1. Excessive ROS formation could damage cell structures, lipids, proteins and nucleic acids, and ultimately could lead to cell death [119]. Different species and tissues have particularities regarding development of oxidative stress and the major detoxifying players. For example, grass species are reported to be less sensitive to oxidative stress during drought and warming compared to legume species [122]. Upregulation only for catalase is reported in heat stressed roots [123] while concerted increase in the activities of several antioxidative enzymes is found in stressed leaves [124,125]. Control of ROS accumulation and detoxification are key processes during abiotic stress phases, which play critical role for yield stability [10]. As ROS protection is common mechanism mobilized in many abiotic stresses including drought [126,127,128,129], heat [10,115,125,130,131] and their combination [122,132], ROS scavenging enzymes and compounds are good candidates for enhanced protection to multiple stress situations. Higher tolerance to drought and/or heat is associated with concerted up-regulation of key detoxifying enzymes in several crop species/varieties leading to better ROS protection along with stability of key metabolic processes like photosynthesis [132] and maintenance of the alternative mitochondrial respiration [123]. Field drought causes an increased oxidative stress during the grain filling period, especially to drought sensitive wheat varieties [127]. The upregulation of the total antioxidant capacity during grain development in heat tolerant wheat genotypes is linked to delayed senescence and better nutrient reserves mobilization [125]. A principal role of the cytosolic ascorbate peroxidase is established for acclimation to combined drought and heat stress [15]. In Table 1 are listed certain leaf proteins involved in the responses to drought and heat with relation to stress tolerance, among which are several antioxidant enzymes such as superoxide dismutase isoforms and ascorbate peroxidase. Enzymes related to ROS protection are systematically found to be upregulated under abiotic stresses in proteomics studies, which are briefly commented below.

5. Reproductive Structures and Yield Formation

The maturation of fruits and seeds under abiotic stresses is highly relevant for a series of the world most important crops including rice, wheat, maize and soybean [145,146,147,148]. The translocation of nutrients and assimilates via xylem and phloem to the reproductive structures (Figure 2H), the remobilization of leaf constituents (Figure 2K) and processes in the maturing fruits including the deposition of storage compounds in the seeds (Figure 2N) are relevant in this context and depend on water availability [146,147,148] and ambient temperature [145,147,148]. Landraces with a high genetic diversity may serve as a helpful basis for breeding crop genotypes with suitable properties in the course of climate change (e.g., stable yields, high quality of harvested products) [148]. Genetic variability in the response to abiotic stresses such as heat and drought were reported for several crop plants indicating that there might still be a potential for further breeding [146,147,148]. Since drought and heat occur often simultaneously, the combined effects of these abiotic stresses are of special relevance [147,148].

6. Proteomics in Search of Molecular Markers for Assisted Selection and Breeding

The potential of proteomics has been increasingly exploited in search of suitable protein markers for assisted selection and breeding, thus complementing the widely used genomic tools [149,150,151,152]. Proteins are direct effectors in the processes related to cell structure and function, as well as in adaptation to the changing environment—underlying the so called phenotypic plasticity [152]. Cell protein composition is highly dynamic and much closer to the plant phenotype than the transcript profiling. Protein and transcript profiles do not necessary correspond to each other due to the complexity of regulation of gene expression (at genetic, transcriptional, translational, and post-translational levels). Plant proteomics has benefited from the technological advances in the field and from the development of databases with partially or fully sequenced plant genomes and expressed sequence tags, necessary for correct protein identification; comprehensive proteome maps of major crops have been established [131,153]. Both gel-based and chromatography-based approaches are applied in plant proteomics as they are complementary. Two-dimensional electrophoresis combined with mass spectrometry detects relatively more abundant proteins like key metabolic enzymes, thus providing essential information about changes in the main metabolic pathways and biological processes affected by the stress, usually in good correlation with metabolomics data; moreover, isoforms and posttranslational modifications of a given protein can be established [153]. Deeper proteome coverage especially for less abundant proteins (signaling, transporters, etc.) is reached by the second generation shotgun proteomics [153,154,155]. Knowledge about dynamic changes of crop proteomes in response to abiotic stresses is regularly reviewed [131,150,152,153,156]. For that reason, our attention is mainly focused on recent proteomic reports addressing drought, heat and combined stress.
Recent proteomic studies on drought response of crops encompass different plant species, such as wheat [138,157], rice [158,159], barley [160], brassica [154], legumes [141,161]. Different types of tissues are studied: roots [141,154,159], root nodules [161], leaves [138,160], roots and leaves compared at seedling stage [157], roots, flag leaves and spikelets at reproductive stage [151]. As the high temperature is particularly detrimental during the reproductive stage, besides the studies on leaf proteome under heat stress in rice [113,162], wheat [163] radish [142], alfalfa [164] and stromal proteins in agave [165], special attention is paid to the reproductive phase [166], source-sink interactions at grain filling [167], grain development and composition [155,160] in cereals, and protein composition of soybean seeds [168] formed under unfavorable temperature conditions. Relatively few proteomic studies deal with combined drought and heat stress [169,170,171]. Current efforts are directed at elucidating the drought adaptations in roots and leaves, the response to heat at reproductive developmental stage, as well as at the early signaling events captured after 4–8 h of drought [154,157], heat [147,163] or combined [169] treatments, including changes in phosphorylation of specific proteins [157,169]. As signal transduction associated, 14-3-3 proteins and calreticulin-like proteins were upregulated in tolerant wheat cultivar under drought stress [157]. In roots of transgenic rice, overexpressing DREB1A, a novel protein containing ricin B lectin domain was found to be highly accumulated, probably with potential role in breeding for drought tolerance [159]. Proteomic findings support and further develop the concept about key mechanisms affected by drought and heat stress and point at some potential protein markers for assisted selection.

7. Conclusions and Outlook

Genetic variability is a prerequisite for breeding plants with an improved heat or drought tolerance [6,7,8,9,145]. Modern techniques including genetic engineering [172] and high-throughput phenotyping [173] may facilitate the production/selection of suitable genotypes. From the facts and concepts reviewed in this paper, it becomes evident that the susceptibility to abiotic stresses is complex and incudes morphological and physiological traits [174,175]. Several important traits for drought and heat tolerance in crop plants are summarized in Table 2. Stress responses can be reversible after the stress period (e.g., leaf orientation, stomatal opening, activation status of Rubisco), partially reversible (e.g., rooting depth, activity of the shoot apical meristem) or irreversible (e.g., senescence of a leaf or a root, deposition of compounds on the leaf surface). In the case of partially reversible and irreversible responses, the effect as such may be irreversible, but it may be partially or fully compensated after the stress period (e.g., xylem functionality, photosynthetically active biomass).
There might be some defined properties, which are directly advantageous for stress-exposed plants (e.g., heat tolerance of Rubisco activase, root and shoot architecture or properties of the leaf surface) [6,144], but in most cases a complex regulatory network including signal perception and transduction must be considered [154]. Although anatomical and physiological properties of the root system are not easily accessible in field experiments, root growth, activity and response to abiotic stresses must be borne in mind for identifying suitable genotypes [27,141,174]. Besides basic characteristics of unstressed plants, especially stress-inducible adaptations in gene expression, protein pattern and physiological properties are important for the stress susceptibility of a genotype [113,162,163]. Heat waves and drought periods occur often simultaneously and should therefore also be addressed in combination in selection procedures [169,170,171].
Several environmental factors are relevant for agronomic practices (e.g., altitude, soil properties, nutrient availability) and can interfere with the responses of crop plants to heat or drought. Such interactions are relevant for selecting genotypes with suitable properties. Therefore it cannot be expected to find “the suitable drought- or heat-tolerant genotype”, but there might be a collection of varieties for various environments. Since genotypes must be selected before the growing season (with or without severe stress phases), experiences from preceding years may serve as a basis. Since more frequent and more severe extreme events including droughts and heat waves must be expected in the course of global change, breeding of crop plants with an improved performance during and after stress periods becomes a key determinant [9,10,11,141,157,175].

Acknowledgments

Experimental work leading to this review was partially supported by Swiss National Science Foundation (NCCR “Climate”, project “Plant and Soil” and SCOPES project “DILPA”).

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

The following abbreviations are used in this manuscript:
P5CS
D-1pyrroline-5-carboxylate synthetase
ROS
Reactive oxygen species

References

  1. IPCC. Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2014. [Google Scholar]
  2. Schär, C.; Vidale, P.L.; Luthi, D.; Frei, C.; Haberli, C.; Liniger, M.A.; Appenzeller, C. The role of increasing temperature variability in European summer heat waves. Nature 2004, 427, 332–336. [Google Scholar] [CrossRef] [PubMed]
  3. Fischer, E.M.; Knutti, R. Anthropogenic contribution to global occurrence of heavy-precipitation and high temperature extremes. Nat. Clim. Chang. 2015, 5, 560–564. [Google Scholar] [CrossRef]
  4. Knutti, R.; Rogelj, J.; Sedlacek, J.; Fischer, E.M. A scientific critique of the two-degree climate change target. Nat. Geosci. 2016, 9, 13–19. [Google Scholar] [CrossRef]
  5. DaMatta, F.M.; Grandis, A.; Arenque, B.C.; Buckeridge, M.S. Impacts of climate changes on crop physiology and food quality. Food Res. Internat. 2010, 43, 1814–1823. [Google Scholar] [CrossRef]
  6. Parry, M.A.J.; Reynolds, M.; Salvucci, M.E.; Raines, C.; Andralojc, P.J.; Zhu, X.G.; Price, G.D.; Condon, A.G.; Furbank, R.T. Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. J. Exp. Bot. 2011, 62, 453–467. [Google Scholar] [PubMed]
  7. Driever, S.M.; Lawson, T.; Andralojc, P.J.; Raines, C.A.; Parry, M.A.J. Natural variation in photosynthetic capacity, growth, and yield in 64 field-grown wheat genotypes. J. Exp. Bot. 2014, 65, 4959–4973. [Google Scholar] [CrossRef] [PubMed]
  8. Krannich, C.T.; Maletzki, L.; Kurowsky, C.; Horn, R. Network candidate genes in breeding for drought tolerant crops. Int. J. Mol. Sci. 2015, 16, 16378–16400. [Google Scholar] [CrossRef] [PubMed]
  9. Vassileva, V.; Signarbieux, C.; Anders, I.; Feller, U. Genotypic variation in drought stress response and subsequent recovery of wheat (Triticum aestivum L.). J. Plant Res. 2011, 124, 147–154. [Google Scholar] [CrossRef] [PubMed]
  10. Siebers, M.H.; Yendrek, C.R.; Drag, D.; Locke, A.M.; Acosta, R.L.; Leakey, A.D.B.; Ainsworth, E.A.; Bernacchi, C.J.; Ort, D.R. Heat waves imposed during early pod development in soybean (Glycine max) cause significant yield loss despite a rapid recovery from oxidative stress. Glob. Chang. Biol. 2015, 21, 3114–3125. [Google Scholar] [CrossRef] [PubMed]
  11. Zwicke, M.; Picon-Cochard, C.; Morvan-Bertrand, A.; Prud’homme, M.-P.; Volaire, F. What functional strategies drive drought survival and recovery of perennial species from upland grassland? Ann. Bot. 2015, 116, 1001–1015. [Google Scholar] [CrossRef] [PubMed]
  12. Narayanan, S.; Mohan, A.; Gill, K.S.; Prasad, P.V.V. Variability of root traits in spring wheat germplasm. PLoS ONE 2014, 9, e100317. [Google Scholar] [CrossRef] [PubMed]
  13. Chaves, M.M.; Maroco, J.P.; Pereira, J.S. Understanding plant responses to drought—From genes to the whole plant. Funct. Plant Biol. 2003, 30, 239–264. [Google Scholar] [CrossRef]
  14. Mittler, R. Abiotic stress, the field environment and stress combination. Trends Plant Sci. 2006, 11, 15–19. [Google Scholar] [CrossRef] [PubMed]
  15. Koussevitzky, S.; Suzuki, N.; Huntington, S.; Armijo, L.; Sha, W.; Cortes, D.; Shulaev, V.; Mittler, R. Ascorbate peroxidase 1 plays a key role in the response of Arabidopsis thaliana to stress combination. J. Biol. Chem. 2008, 283, 34197–34203. [Google Scholar] [CrossRef] [PubMed]
  16. Shao, H.B.; Chu, L.Y.; Jaleel, C.A.; Zhao, C.X. Water-deficit stress-induced anatomical changes in higher plants. C R. Biol. 2008, 331, 215–225. [Google Scholar] [CrossRef] [PubMed]
  17. Hasanuzzaman, M.; Nahar, K.; Alam, M.M.; Roychowdhury, R.; Fujita, M. Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int. J. Mol. Sci. 2013, 14, 9643–9684. [Google Scholar] [CrossRef] [PubMed]
  18. Feller, U.; Vaseva, I.I. Extreme climatic events: Impacts of drought and high temperature on physiological processes in agronomically important plants. Front. Environ. Sci. 2014, 2, 39. [Google Scholar] [CrossRef]
  19. Shanker, A.K.; Maheswari, M.; Yadav, S.K.; Desai, S.; Bhanu, D.; Attal, N.B.; Venkateswarlu, B. Drought stress responses in crops. Funct. Integr. Genomics 2014, 14, 11–22. [Google Scholar] [CrossRef] [PubMed]
  20. Hatfield, J.L.; Prueger, J.H. Temperature extremes: Effect on plant growth and development. Weather Clim. Extremes 2015, 10, 4–10. [Google Scholar] [CrossRef]
  21. Kazan, K.; Lyons, R. The link between flowering time and stress tolerance. J. Exp. Bot. 2016, 67, 47–60. [Google Scholar] [CrossRef] [PubMed]
  22. Schulze, E.D.; Mooney, H.A.; Sala, O.E.; Jobbagy, E.; Buchmann, N.; Bauer, G.; Canadell, J.; Jackson, R.B.; Loreti, J.; Oesterheld, M.; et al. Rooting depth, water availability, and vegetation cover along an aridity gradient in Patagonia. Oecologia 1996, 108, 503–511. [Google Scholar] [CrossRef]
  23. Signarbieux, C.; Feller, U. Effects of an extended drought period on physiological properties of grassland species in the field. J. Plant Res. 2012, 125, 251–261. [Google Scholar] [CrossRef] [PubMed]
  24. Bollig, C.; Feller, U. Impacts of drought stress on water relations and carbon assimilation in grassland species at different altitudes. Agric. Ecosyst. Environ. 2014, 188, 212–220. [Google Scholar] [CrossRef]
  25. Padilla, F.M.; Pugnaire, F.I. Rooting depth and soil moisture control Mediterranean woody seedling survival during drought. Funct. Ecol. 2007, 21, 489–495. [Google Scholar] [CrossRef]
  26. Vassileva, V.; Demirevska, K.; Simova-Stoilova, L.; Petrova, T.; Tsenov, N.; Feller, U. Long-term field drought affects leaf protein pattern and chloroplast ultrastructure of winter wheat in a cultivar-specific manner. J. Agric. Crop Sci. 2012, 198, 104–117. [Google Scholar] [CrossRef]
  27. Kashiwagi, J.; Morito, Y.; Jitsuyama, Y.; An, P.; Inoue, T.; Inagaki, M. Effects of root water uptake efficiency on soil water utilization in wheat (Triticum aestivum L.) under severe drought environments. J. Agric. Crop Sci. 2015, 201, 161–172. [Google Scholar] [CrossRef]
  28. Reader, R.J.; Jalili, A.; Grime, J.P.; Spencer, R.E.; Matthews, N. A comparative-study of plasticity in seedling rooting depth in drying soil. J. Ecol. 1993, 81, 543–550. [Google Scholar] [CrossRef]
  29. Grieder, C.; Trachsel, S.; Hund, A. Early vertical distribution of roots and its association with drought tolerance in tropical maize. Plant Soil 2014, 377, 295–308. [Google Scholar] [CrossRef]
  30. Zhan, A.; Schneider, H.; Lynch, J.P. Reduced lateral root branching density improves drought tolerance in maize. Plant Physiol. 2015, 168, 1603–1615. [Google Scholar] [CrossRef] [PubMed]
  31. Reynolds, M.; Tuberosa, R. Translational research impacting on crop productivity in drought-prone environments. Curr. Opin. Plant. Biol. 2008, 11, 171–179. [Google Scholar] [CrossRef] [PubMed]
  32. Comas, L.H.; Becker, S.R.; Von Mark, V.C.; Byrne, P.F.; Dierig, D.A. Root traits contributing to plant productivity under drought. Front. Plant Sci. 2013, 4, 442. [Google Scholar] [CrossRef] [PubMed]
  33. Paez-Garcia, A.; Motes, C.M.; Scheible, W.R.; Chen, R.; Blancaflor, E.B.; Monteros, M.J. Root traits and phenotyping strategies for plant improvement. Plants 2015, 4, 334–355. [Google Scholar] [CrossRef] [PubMed]
  34. Kano, M.; Inukai, Y.; Kitano, H.; Yamauchi, A. Root plasticity as the key root trait for adaptation to various intensities of drought stress in rice. Plant Soil 2011, 342, 117–128. [Google Scholar] [CrossRef]
  35. Babe, A.; Lavigne, T.; Severin, J.P.; Nagel, K.A.; Walter, A.; Chaumont, F.; Batoko, H.; Beeckman, T.; Draye, X. Repression of early lateral root initiation events by transient water deficit in barley and maize. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 2012, 367, 1534–1541. [Google Scholar] [CrossRef] [PubMed]
  36. Wasson, A.P.; Richards, R.A.; Chatrath, R.; Misra, S.C.; Prasad, S.S.; Rebetzke, G.J.; Kirkegaard, J.A.; Christopher, J.; Watt, M. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J. Exp. Bot. 2012, 63, 3485–3498. [Google Scholar] [CrossRef] [PubMed]
  37. Clarke, S.J.; Lamont, K.J.; Pan, H.Y.; Barry, L.A.; Hall, A.; Rogiers, S.Y. Spring root-zone temperature regulates root growth, nutrient uptake and shoot growth dynamics in grapevines. Aust. J. Grape Wine Res. 2015, 21, 479–489. [Google Scholar] [CrossRef]
  38. Nippert, J.B.; Holdo, R.M. Challenging the maximum rooting depth paradigm in grasslands and savannas. Funct. Ecol. 2015, 29, 739–745. [Google Scholar] [CrossRef]
  39. Zhang, H.M.; Jennings, A.; Barlow, P.W.; Forde, B.G. Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. USA 1999, 96, 6529–6534. [Google Scholar] [CrossRef] [PubMed]
  40. Walch-Liu, P.; Ivanov, I.I.; Filleur, S.; Gan, Y.B.; Remans, T.; Forde, B.G. Nitrogen regulation of root branching. Ann. Bot. 2006, 97, 875–881. [Google Scholar] [CrossRef] [PubMed]
  41. Desnos, T. Root branching responses to phosphate and nitrate. Curr. Opin. Plant Biol. 2008, 11, 82–87. [Google Scholar] [CrossRef] [PubMed]
  42. Zhu, J.M.; Kaeppler, S.M.; Lynch, J.P. Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor. Appl. Genet. 2005, 111, 688–695. [Google Scholar] [PubMed]
  43. Forde, B.; Lorenzo, H. The nutritional control of root development. Plant Soil 2001, 232, 51–68. [Google Scholar] [CrossRef]
  44. Sanchez-Rodriguez, E.; Rubio-Wilhelmi, M.M.; Blasco, B.; Constan-Aguilar, C.; Romero, L.; Ruiz, J.M. Variation in the use efficiency of N under moderate water deficit in tomato plants (Solanum lycopersicum) differing in their tolerance to drought. Acta Physiol. Plant. 2011, 33, 1861–1865. [Google Scholar] [CrossRef]
  45. Ge, T.D.; Sun, N.B.; Bai, L.P.; Tong, C.L.; Sui, F.G. Effects of drought stress on phosphorus and potassium uptake dynamics in summer maize (Zea mays) throughout the growth cycle. Acta Physiol. Plant. 2012, 34, 2179–2186. [Google Scholar] [CrossRef]
  46. Nawaz, F.; Ahmad, R.; Waraich, E.A.; Naeem, M.S.; Shabbir, R.N. Nutrient uptake, physiological responses, and yield attributes of wheat (Triticum aestivum L.) exposed to early and late drought stress. J. Plant Nutr. 2012, 35, 961–974. [Google Scholar]
  47. Ren, H.B.; Wei, K.F.; Jia, W.S.; Davies, W.J.; Zhang, J.H. Modulation of root signals in relation to stomatal sensitivity to root-sourced abscisic acid in drought-affected plants. J. Integrat. Plant Biol. 2007, 49, 1410–1420. [Google Scholar] [CrossRef]
  48. Merewitz, E.B.; Gianfagna, T.; Huang, B.R. Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J. Exp. Bot. 2011, 62, 5311–5333. [Google Scholar] [CrossRef] [PubMed]
  49. De Ollas, C.; Hernando, B.; Arbona, V.; Gomez-Cadenas, A. Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol. Plant. 2013, 147, 296–306. [Google Scholar] [CrossRef] [PubMed]
  50. Allario, T.; Brumos, J.; Colmenero-Flores, J.M.; Iglesias, D.J.; Pina, J.A.; Navarro, L.; Talon, M.; Ollitrault, P.; Morillon, R. Tetraploid Rangpur lime rootstock increases drought tolerance via enhanced constitutive root abscisic acid production. Plant Cell Environ. 2013, 36, 856–868. [Google Scholar] [CrossRef] [PubMed]
  51. Larrainzar, E.; Molenaar, J.A.; Wienkoop, S.; Gil-Quintana, E.; Alibert, B.; Limami, A.M.; Arrese-Igor, C.; Gonzalez, E.M. Drought stress provokes the down-regulation of methionine and ethylene biosynthesis pathways in Medicago truncatula roots and nodules. Plant Cell Environ. 2014, 37, 2051–2063. [Google Scholar] [CrossRef] [PubMed]
  52. Karsten, H.D.; MacAdam, J.W. Effect of drought on growth, carbohydrates, and soil water use by perennial ryegrass, tall fescue, and white clover. Crop Sci. 2001, 41, 156–166. [Google Scholar] [CrossRef]
  53. Erice, G.; Irigoyen, J.J.; Sanchez-Diaz, M.; Avice, J.C.; Ourry, A. Effect of drought, elevated CO2 and temperature on accumulation of N and vegetative storage proteins (VSP) in taproot of nodulated alfalfa before and after cutting. Plant Sci. 2007, 172, 903–912. [Google Scholar] [CrossRef]
  54. Hoffmann, C.M. Adaptive responses of Beta vulgaris L. and Cichorium intybus L. root and leaf forms to drought stress. J. Agric. Crop Sci. 2014, 200, 108–118. [Google Scholar]
  55. Kivuva, B.M.; Githiri, S.M.; Yencho, G.C.; Sibiya, J. Screening sweetpotato genotypes for tolerance to drought stress. Field Crops Res. 2015, 171, 11–22. [Google Scholar] [CrossRef]
  56. Ruizlozano, J.M.; Azcon, R.; Gomez, M. Effects of arbuscular-mycorrhizal glomus species on drought tolerance—Physiological and nutritional plant-responses. Appl. Environ. Microbiol. 1995, 61, 456–460. [Google Scholar]
  57. Roberts, S.K. Regulation of K+ channels in maize roots by water stress and abscisic acid. Plant Physiol. 1998, 116, 145–153. [Google Scholar] [CrossRef]
  58. Pilot, G.; Gaymard, F.; Mouline, K.; Cherel, I.; Sentenac, H. Regulated expression of Arabidopsis Shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol. Biol. 2003, 51, 773–787. [Google Scholar] [CrossRef] [PubMed]
  59. Wegner, L.H.; Zimmermann, U. Hydraulic conductance and K+ transport into the xylem depend on radial volume flow, rather than on xylem pressure, in roots of intact, transpiring maize seedlings. New Phytol. 2009, 181, 361–373. [Google Scholar] [CrossRef] [PubMed]
  60. Wegner, L.H.; Stefano, G.; Shabala, L.; Rossi, M.; Mancuso, S.; Shabala, S. Sequential depolarization of root cortical and stelar cells induced by an acute salt shock—Implications for Na+ and K+ transport into xylem vessels. Plant Cell Environ. 2011, 34, 859–869. [Google Scholar] [CrossRef] [PubMed]
  61. Al-Karaki, G.N. Benefit, cost and water-use efficiency of arbuscular mycorrhizal durum wheat grown under drought stress. Mycorrhiza 1998, 8, 41–45. [Google Scholar] [CrossRef]
  62. Kozlowski, T.T.; Pallardy, S.G. Acclimation and adaptive responses of woody plants to environmental stresses. Bot. Rev. 2002, 68, 270–334. [Google Scholar] [CrossRef]
  63. Al-Karaki, G.; McMichael, B.; Zak, J. Field response of wheat to arbuscular mycorrhizal fungi and drought stress. Mycorrhiza 2004, 14, 263–269. [Google Scholar] [CrossRef] [PubMed]
  64. Valentine, A.J.; Mortimer, P.E.; Lintnaar, A.; Borgo, R. Drought responses of arbuscular mycorrhizal grapevines. Symbiosis 2006, 41, 127–133. [Google Scholar]
  65. Subramanian, K.S.; Santhanakrishnan, P.; Balasubramanian, P. Responses of field grown tomato plants to arbuscular mycorrhizal fungal colonization under varying intensities of drought stress. Sci. Hort. 2006, 107, 245–253. [Google Scholar] [CrossRef]
  66. Borowicz, V.A. The impact of arbuscular mycorrhizal fungi on strawberry tolerance to root damage and drought stress. Pedobiologia 2010, 53, 265–270. [Google Scholar] [CrossRef]
  67. Barzana, G.; Aroca, R.; Paz, J.A.; Chaumont, F.; Martinez-Ballesta, M.C.; Carvajal, M.; Ruiz-Lozano, J.M. Arbuscular mycorrhizal symbiosis increases relative apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann. Bot. 2012, 109, 1009–1017. [Google Scholar] [CrossRef] [PubMed]
  68. Li, T.; Lin, G.; Zhang, X.; Chen, Y.L.; Zhang, S.B.; Chen, B.D. Relative importance of an arbuscular mycorrhizal fungus (Rhizophagus intraradices) and root hairs in plant drought tolerance. Mycorrhiza 2014, 24, 595–602. [Google Scholar] [CrossRef] [PubMed]
  69. Nouri, E.; Breuillin-Sessoms, F.; Feller, U.; Reinhardt, D. Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 2014, 9, e90841. [Google Scholar] [CrossRef] [PubMed]
  70. Auge, R.M.; Toler, H.D.; Saxton, A.M. Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: A meta-analysis. Mycorrhiza 2015, 25, 13–24. [Google Scholar] [PubMed]
  71. Jensen, E.S.; Nielsen, H.H. How can increased use of biological N2 fixation in agriculture benefit the environment? Plant Soil 2003, 252, 177–186. [Google Scholar] [CrossRef]
  72. Crews, T.E.; Peoples, M.B. Legume versus fertilizer sources of nitrogen: Ecological tradeoffs and human needs. Agric. Ecosyst. Environ. 2004, 102, 279–297. [Google Scholar] [CrossRef]
  73. Naudin, C.; Corre-Hellou, G.; Voisin, A.S.; Oury, V.; Salon, C.; Crozat, Y.; Jeuffroy, M.H. Inhibition and recovery of symbiotic N-2 fixation by peas (Pisum sativum L.) in response to short-term nitrate exposure. Plant Soil 2011, 346, 275–287. [Google Scholar]
  74. Graham, P.H.; Vance, C.P. Legumes: importance and constraints to greater use. Plant Physiol. 2003, 131, 872–877. [Google Scholar] [CrossRef] [PubMed]
  75. Biswas, B.; Scott, P.T.; Gresshoff, P.M. Tree legumes as feed—Stock for sustainable biofuel production: opportunities and challenges. J. Plant Physiol. 2011, 168, 1877–1884. [Google Scholar] [CrossRef] [PubMed]
  76. Araújo, S.S.; Beebe, S.; Crespi, M.; Delbreil, B.; González, E.M.; Gruber, V.; Lejeune-Henaut, I.; Link, W.; Monteros, M.J.; Prats, E.; et al. Abiotic stress responses in legumes: Strategies used to cope with environmental challenges. Crit. Rev. Plant Sci. 2015, 34, 237–280. [Google Scholar] [CrossRef]
  77. González, E.M.; Larrainzar, E.; Marino, D.; Wienkoop, S.; Gil-Quintana, E.; Arrese-Igor, C. Physiological responses of N2-fixing legumes to water limitation. In Legume Nitrogen Fixation in a Changing Environment; Springer International Publishing: Berlin, Germany; Heidelberg, Germany, 2015; pp. 5–33. [Google Scholar]
  78. Vadez, V.; Sinclair, T.R.; Serraj, R. Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiol. Plant. 2000, 110, 215–223. [Google Scholar] [CrossRef]
  79. Streeter, J.G. Effects of drought on nitrogen fixation in soybean root nodules. Plant Cell Environ. 2003, 26, 1199–1204. [Google Scholar] [CrossRef]
  80. Boonkerd, N.; Weaver, R.W. Survival of cowpea rhizobia in soil as affected by soil temperature and moisture. Appl. Environ. Microbiol. 1982, 43, 585–589. [Google Scholar] [PubMed]
  81. Miller, M.S.; Pepper, I.L. Survival of a fast-growing strain of lupin rhizobia in Sonoran Desert soils. Soil Biol. Biochem. 1988, 20, 323–327. [Google Scholar] [CrossRef]
  82. Williams, P.M.; de Mallorca, M.S. Effect of osmotically induced leaf moisture stress on nodulation and nitrogenase activity of Glycine max. Plant Soil 1984, 80, 267–283. [Google Scholar] [CrossRef]
  83. Morieri, G.; Martinez, E.A.; Jarynowski, A.; Driguez, H.; Morris, R.; Oldroyd, G.E.; Downie, J.A. Host-specific Nod-factors associated with Medicago truncatula nodule infection differentially induce calcium influx and calcium spiking in root hairs. New Phytol. 2013, 200, 656–662. [Google Scholar] [CrossRef] [PubMed]
  84. Worrall, V.S.; Roughley, R.J. The effect of moisture stress on infection of Trifolium subterraneum L. by Rhizobium trifolii Dang. J. Exp. Bot. 1976, 27, 1233–1241. [Google Scholar] [CrossRef]
  85. Kirova, E.; Tzvetkova, N.; Vaseva, I.; Ignatov, G. Photosynthetic responses of nitrate-fed and nitrogen-fixing soybeans to progressive water stress. J. Plant Nutr. 2008, 31, 445–458. [Google Scholar] [CrossRef]
  86. Marquez-Garcia, B.; Shaw, D.; Cooper, J.W.; Karpinska, B.; Quain, M.D.; Makgopa, E.M.; Kunert, K.; Foyer, C.H. Redox markers for drought-induced nodule senescence, a process occurring after drought-induced senescence of the lowest leaves in soybean (Glycine max). Ann. Bot. 2015, 116, 497–510. [Google Scholar] [CrossRef] [PubMed]
  87. Ladrera, R.; Marino, D.; Larrainzar, E.; Gonzalez, E.M.; Arrese-Igor, C. Reduced carbon availability to bacteroids and elevated ureides in nodules, but not in shoots, are involved in the nitrogen fixation response to early drought in soybean. Plant Physiol. 2007, 145, 539–546. [Google Scholar] [CrossRef] [PubMed]
  88. Baral, B.; Izaguirre-Mayoral, M.L. Early signaling, synthesis, transport and metabolism of ureides. J. Plant Physiol. 2016, 193, 97–109. [Google Scholar] [CrossRef] [PubMed]
  89. Sinclair, T.R.; Serraj, R. Legume nitrogen-fixation and drought. Nature 1995, 378, 344. [Google Scholar] [CrossRef]
  90. Serraj, R.; Sinclair, T.R.; Purcell, L.C. Symbiotic N2 fixation response to drought. J. Exp. Bot. 1999, 50, 143–155. [Google Scholar] [CrossRef]
  91. Charlson, D.V.; Korth, K.L.; Purcell, L.C. Allantoate amidohydrolase transcript expression is independent of drought tolerance in soybean. J. Exp. Bot. 2009, 60, 847–851. [Google Scholar] [CrossRef] [PubMed]
  92. Arrese-Igor, C.; González, E.M.; Marino, D.; Ladrera, R.; Larrainzar, E.; Gil-Quintana, E. Physiological responses of legume nodules to drought. Plant Stress 2011, 5, 24–31. [Google Scholar]
  93. Kirova, E.; Nedeva, D.; Nikolova, A.; Ignatov, G. Changes in the electrophoretic spectra of antioxidant enzymes in nitrate-fed and nitrogen-fixing soybean subjected to gradual water stress. Acta Agron. Hung. 2005, 52, 323–332. [Google Scholar] [CrossRef]
  94. Sassi, S.; Gonzalez, E.M.; Aydi, S.; Arrese-Igor, C.; Abdelly, C. Tolerance of common bean to long-term osmotic stress is related to nodule carbon flux and antioxidant defenses: Evidence from two cultivars with contrasting tolerance. Plant Soil 2008, 312, 39–48. [Google Scholar] [CrossRef]
  95. Kaur, S.; Gupta, A.K.; Kaur, N.; Sandhu, J.S.; Gupta, S.K. Antioxidative enzymes and sucrose synthase contribute to cold stress tolerance in chickpea. J. Agron. Crop Sci. 2009, 195, 393–397. [Google Scholar] [CrossRef]
  96. Shabala, S.; White, R.G.; Djordjevic, M.A.; Ruan, Y.L.; Mathesius, U. Root-to-shoot signalling: Integration of diverse molecules, pathways and functions. Funct. Plant Biol. 2016, 43, 87–104. [Google Scholar]
  97. Kaufmann, I.; Schulze-Till, T.; Schneider, H.U.; Zimmermann, U.; Jakob, P.; Wegner, L.H. Functional repair of embolized vessels in maize roots after temporal drought stress, as demonstrated by magnetic resonance imaging. New Phytol. 2009, 184, 245–256. [Google Scholar] [CrossRef] [PubMed]
  98. Trifilo, P.; Nardini, A.; Raimondo, F.; Lo Gullo, M.A.; Salleo, S. Ion-mediated compensation for drought-induced loss of xylem hydraulic conductivity in field-growing plants of Laurus nobilis. Funct. Plant Biol. 2011, 38, 606–613. [Google Scholar] [CrossRef]
  99. Brodersen, C.R.; McElrone, A.J.; Choat, B.; Lee, E.F.; Shackel, K.A.; Matthews, M.A. In vivo visualizations of drought-induced embolism spread in Vitis vinifera. Plant Physiol. 2013, 161, 1820–1829. [Google Scholar] [CrossRef] [PubMed]
  100. Sevanto, S. Phloem transport and drought. J. Exp. Bot. 2014, 65, 1751–1759. [Google Scholar] [CrossRef] [PubMed]
  101. Rose, T.J.; Raymond, C.A.; Bloomfield, C.; King, G.J. Perturbation of nutrient source-sink relationships by post-anthesis stresses in differential accumulation of nutrients in wheat grain. J. Plant Nutr. 2015, 178, 89–98. [Google Scholar] [CrossRef]
  102. Feller, U.; Anders, I.; Wei, S. Effects of PEG-induced water deficit in Solanum nigrum on Zn and Ni uptake and translocation in splot root systems. Plants 2015, 4, 284–297. [Google Scholar] [CrossRef] [PubMed]
  103. Feller, U. Drought stress and carbon assimilation in a warming climate: Reversible and irreversible impacts. J. Plant Physiol. 2016. [Google Scholar] [CrossRef] [PubMed]
  104. Blum, A.; Golan, G.; Mayer, J.; Sinmena, B. The effect of dwarfing genes on sorghum grain filling from remobilized stem reserves under stress. Field Crops Res. 1997, 52, 43–54. [Google Scholar] [CrossRef]
  105. Pinheiro, C.; Passarinho, J.A.; Ricardo, C.P. Effect of drought and rewatering on the metabolism of Lupinus albus organs. J. Plant Physiol. 2004, 161, 1203–1210. [Google Scholar] [CrossRef] [PubMed]
  106. Flexas, J.; Bota, J.; Loreto, F.; Cornic, G.; Sharkey, T.D. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C(3) plants. Biol. Plant. 2004, 6, 269–279. [Google Scholar] [CrossRef] [PubMed]
  107. Boughalleb, F.; Hajlaoui, H.; Denden, M. Effect of salt stress on growth, water relations, solute composition and photosynthetic capacity of the xero-halophyte Nitraria retusa (L.). Environ. Res. J. 2012, 6, 1–13. [Google Scholar]
  108. Shabala, L.; Mackay, A.; Tian, Y.; Jacobsen, S.E.; Zhou, D.W.; Shabala, S. Oxidative stress protection and stomatal patterning as components of salinity tolerance mechanism in quinoa (Chenopodium quinoa). Physiol. Plant. 2012, 146, 26–38. [Google Scholar] [CrossRef] [PubMed]
  109. Shabala, S. Learning from halophytes: Physiological basis and strategies to improve abiotic stress tolerance in crops. Ann. Bot. 2013, 112, 1209–1221. [Google Scholar] [CrossRef] [PubMed]
  110. Parida, A.K.; Veerabathini, S.K.; Kumari, A.; Agarwal, P.K. Physiological, anatomical and metabolic implications of salt tolerance in the halophyte Salvadora persica under hydroponic culture condition. Front. Plant Sci. 2016, 7, 351. [Google Scholar] [CrossRef] [PubMed]
  111. Farooq, M.; Hussain, M.; Wahid, A.; Siddique, K.H.M. Drought stress in plants: An overview. In Plant Responses to Drought Stress; Springer: Berlin, Germany; Heidelberg, Germany, 2012; pp. 1–33. [Google Scholar]
  112. Xu, Z.Z.; Zhou, G.S.; Shimizu, H. Effects of soil drought with nocturnal warming on leaf stomatal traits and mesophyll cell ultrastructure of a perennial grass. Crop Sci. 2009, 49, 1843–1851. [Google Scholar] [CrossRef]
  113. Das, A.; Mukhopadhyay, M.; Sarkar, B.; Saha, D.; Mondal, T.K. Influence of drought stress on cellular ultrastructure and antioxidant system in tea cultivars with different drought sensitivities. J. Environ. Biol. 2015, 36, 875–882. [Google Scholar] [PubMed]
  114. Vani, B.; Saradhi, P.P.; Mohanty, P. Alteration in chloroplast structure and thylakoid membrane composition due to in vivo heat treatment of rice seedlings: Correlation with the functional changes. J. Plant Physiol. 2001, 158, 583–592. [Google Scholar] [CrossRef]
  115. Munné-Bosch, S.; Jubany-Marí, T.; Alegre, L. Drought-induced senescence is characterized by a loss of antioxidant defences in chloroplasts. Plant, Cell Environ. 2001, 24, 1319–1327. [Google Scholar] [CrossRef]
  116. Vassileva, V.; Simova-Stoilova, L.; Demirevska, K.; Feller, U. Variety-specific response of wheat (Triticum aestivum L.) leaf mitochondria to drought stress. J. Plant Res. 2009, 122, 445–454. [Google Scholar] [PubMed]
  117. Grigorova, B.; Vassileva, V.; Klimchuk, D.; Vaseva, I.; Demirevska, K.; Feller, U. Drought, high temperature, and their combination affect ultrastructure of chloroplasts and mitochondria in wheat (Triticum aestivum L.) leaves. J. Plant Interact. 2012, 7, 204–213. [Google Scholar] [CrossRef]
  118. Smirnoff, N. The role of active oxygen in the response of plants to water deficit and dessication. New Phytol. 1993, 125, 27–58. [Google Scholar] [CrossRef]
  119. Gechev, T.S.; Van Breusegem, F.; Stone, J.M.; Denev, I.; Laloi, C. Reactive oxygen species as signals thet modulate plant stress responses and programmed cell death. BioEssays 2006, 28, 1091–1101. [Google Scholar] [CrossRef] [PubMed]
  120. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930. [Google Scholar] [CrossRef] [PubMed]
  121. Hasanuzzaman, M.; Hossain, M.A.; Da Silva, J.A.T.; Fujita, M. Plant response and tolerance to abiotic oxidative stress: Antioxidant defense is a key factor (Book Chapter). In Crop Stress and Its Management: Perspectives and Strategies; Springer Netherlands: Dordrecht, The Netherlands, 2012; pp. 261–315. [Google Scholar]
  122. AbdElgawad, H.; Farfan-Vignolo, E.R.; de Vosa, D.; Asard, H. Elevated CO2 mitigates drought and temperature-induced oxidative stress differently in grasses and legumes. Plant Sci. 2015, 231, 1–10. [Google Scholar] [CrossRef] [PubMed]
  123. Xu, Y.; Burgess, P.; Huang, B. Root antioxidant mechanisms in relation to root thermotolerance in perennial grass species contrasting in heat tolerance. PLoS ONE 2015, 10, e0138268. [Google Scholar] [CrossRef] [PubMed]
  124. Du, H.; Zhoua, P.; Huang, B. Antioxidant enzymatic activities and gene expression associated with heat tolerance in a cool-season perennial grass species. Environ. Exp. Bot. 2013, 87, 159–166. [Google Scholar] [CrossRef]
  125. Khanna-Chopra, R.; Chauhan, S. Wheat cultivars differing in heat tolerance show a differential response to oxidative stress during monocarpic senescence under high temperature stress. Protoplasma 2015, 252, 1241–1251. [Google Scholar] [CrossRef] [PubMed]
  126. Simova-Stoilova, L.; Demirevska, K.; Petrova, T.; Tsenov, N.; Feller, U. Antioxidative protection in wheat varieties under severe recoverable drought at seedling stage. Plant Soil Environ. 2008, 54, 529–536. [Google Scholar]
  127. Simova-Stoilova, L.; Demirevska, K.; Petrova, T.; Tsenov, N.; Feller, U. Antioxidative protection and proteolytic activity in tolerant and sensitive wheat (Triticum aestivum L.) varieties subjected to long-term field drought. Plant Growth Regul. 2009, 58, 107–117. [Google Scholar]
  128. Bazargani, M.M.; Sarhadi, E.; Bushehri, A.S.; Matros, A.; Mock, H.P.; Naghavi, M.R.; Hajihoseini, V.; Mardi, M.; Hajirezaei, M.R.; Moradi, F.; et al. A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J. Proteomics 2011, 74, 1959–1973. [Google Scholar] [CrossRef] [PubMed]
  129. Vaseva, I.; Akiscan, Y.; Simova-Stoilova, L.; Kostadinova, A.; Nenkova, R.; Anders, I.; Feller, U.; Demirevska, K. Antioxidant response to drought in red and white clover. Acta Physiol. Plant. 2012, 34, 1689–1699. [Google Scholar] [CrossRef]
  130. Wilson, R.A.; Sangha, M.K.; Banga, S.S.; Atwal, A.K.; Gupta, S. Heat stress tolerance in relation to oxidative stress and antioxidants in Brassica juncea. J. Environ. Biol. 2014, 35, 383–387. [Google Scholar] [PubMed]
  131. Hu, X.; Li, Y.; Li, C.; Yang, H.; Wang, W.; Lu, M. Characterization of small heat shock proteins associated with maize tolerance to combined drought and heat stress. J. Plant Growth Regul. 2010, 29, 455–464. [Google Scholar] [CrossRef]
  132. Signorelli, S.; Casaretto, E.; Sainz, M.; Díaz, P.; Monza, J.; Borsani, O. Antioxidant and photosystem II responses contribute to explain the drought—Heat contrasting tolerance of two forage legumes. Plant Physiol. Biochem. 2013, 70, 195–203. [Google Scholar] [CrossRef] [PubMed]
  133. Moshelion, M.; Halperin, O.; Wallach, R.; Oren, R.; Way, D.A. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: Crop water-use efficiency, growth and yield. Plant Cell Environ. 2015, 38, 1785–1793. [Google Scholar] [CrossRef] [PubMed]
  134. Close, T.J. Dehydrins: A commonality in the response of plants to dehydration and low temperature. Physiol. Plant. 1997, 100, 291–296. [Google Scholar] [CrossRef]
  135. Volaire, F.; Lelievre, F. Drought survival in Dactylis glomerata and Festuca arundinacea under similar rooting conditions in tubes. Plant Soil 2001, 229, 225–234. [Google Scholar] [CrossRef]
  136. Vaseva, I.I.; Anders, I.; Feller, U. Identification and expression of different dehydrin subclasses involved in the drought response of Trifolium repens. J. Plant Physiol. 2014, 171, 213–224. [Google Scholar] [CrossRef] [PubMed]
  137. Salvucci, M.E. Association of Rubisco activase with chaperonin-60 beta: A possible mechanism for protecting photosynthesis during heat stress. J. Exp. Bot. 2008, 58, 1923–1933. [Google Scholar]
  138. Cheng, Z.; Dong, K.; Ge, P.; Bian, Y.; Dong, L.; Deng, X.; Li, X.; Yan, Y. Identification of leaf proteins differentially accumulated between wheat cultivars distinct in their levels of drought tolerance. PLoS ONE 2015, 10, e0125302. [Google Scholar] [CrossRef] [PubMed]
  139. Scharf, K.D.; Berberich, T.; Ebersberger, I.; Nover, L. The plant heat stress transcription factor (Hsf) family: Structure, function and evolution. Biochim. Biophys. Acta 2012, 1819, 104–119. [Google Scholar] [CrossRef] [PubMed]
  140. Wang, X.; Dinler, B.S.; Vignjevic, M.; Jacobsen, S.; Wollenweber, B. Physiological and proteome studies of responses to heat stress during grain filling in contrasting wheat cultivars. Plant Sci. 2015, 230, 33–50. [Google Scholar] [CrossRef] [PubMed]
  141. Sengupta, D.; Kannan, M.; Reddy, A.R. A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek. Planta 2011, 233, 1111–1127. [Google Scholar] [CrossRef] [PubMed]
  142. Zhang, Y.; Xu, L.; Zhu, X.; Gong, Y.; Xiang, F.; Sun, X.; Liu, L. Proteomic analysis of heat stress response in leaves of radish (Raphanus sativus L.). Plant Mol. Biol. Rep. 2013, 31, 195–203. [Google Scholar]
  143. Su, M.; Li, X.F.; Ma, X.Y.; Peng, X.J.; Zhao, A.G.; Cheng, L.Q.; Chen, S.Y.; Liu, G.S. Cloning two P5CS genes from bioenergy sorghum and their expression profiles under abiotic stresses and MeJA treatment. Plant Sci. 2011, 181, 652–659. [Google Scholar] [CrossRef] [PubMed]
  144. Salvucci, M.E.; Crafts-Brandner, S.J. Relationship between the heat tolerance of photosynthesis and the thermal stability of rubisco activase in plants from contrasting thermal environments. Plant Physiol. 2004, 134, 1460–1470. [Google Scholar] [CrossRef] [PubMed]
  145. Nguyen, C.T.; Singh, V.; van Oosterom, E.J.; Chapman, S.C.; Jordan, D.R.; Hammer, G.L. Genetic variability in high temperature effects on seed-set in sorgum. Funct. Plant Biol. 2013, 40, 439–448. [Google Scholar] [CrossRef]
  146. Balla, K.; Bencze, S.; Bonis, P.; Arendas, T.; Veisz, O. Changes in the photosynthetic efficiency of winter wheat in response to abiotic stress. Centr. Eur. J. Biol. 2014, 9, 519–530. [Google Scholar] [CrossRef]
  147. Jagadish, K.S.V.; Kadam, N.N.; Xiao, G.; Melgar, R.J.; Bahuguna, R.N.; Quinones, C.; Tamilselvan, A.; Prasad, P.V.V. Agronomic and physiological responses to high temperature, drought, and elevated CO2 interactions in cereals. Adv. Agron. 2014, 127, 111–156. [Google Scholar]
  148. Lopes, M.S.; El-Basyoni, I.; Baenziger, P.S.; Singh, S.; Royo, C.; Ozbek, K.; Aktas, H.; Ozer, E.; Ozdemir, F.; Manickavelu, A.; et al. Exploiting genetic diversity from landraces in wheat breeding for adaptation to climate change. J. Exp. Bot. 2015, 66, 3477–3486. [Google Scholar] [CrossRef] [PubMed]
  149. Roy, A.; Rushton, P.J.; Rohila, J.S. The potential of proteomics te chnologies for crop improvement under drought conditions. Crit. Rev. Plant Sci. 2011, 30, 471–490. [Google Scholar] [CrossRef]
  150. Abreu, I.A.; Farinha, A.P.; Negrão, S.; Gonçalves, N.; Fonseca, C.; Rodrigues, M.; Batista, R.; Saibo, N.J.M.; Oliveira, M.M. Coping with abiotic stress: Proteome changes for crop improvement. J. Proteomics 2013, 93, 145–168. [Google Scholar]
  151. Raorane, M.L.; Pabuayon, I.M.; Varadarajan, A.R.; Mutte, S.K.; Kumar, A.; Treumann, A.; Kohli, A. Proteomic insights into the role of the large-effect QTL qDTY12.1 for rice yield under drought. Mol. Breed. 2015, 35, 139. [Google Scholar]
  152. Kosová, K.; Vítámvás, P.; Urban, M.O.; Klíma, M.; Roy, A.; Prášil, I.T. Biological networks underlying abiotic stress tolerance in temperate crops—A proteomic perspective. Int. J. Mol. Sci. 2015, 16, 20913–20942. [Google Scholar]
  153. Hashiguchi, A.; Ahsan, N.; Komatsu, S. Proteomics application of crops in the context of climatic changes. Food Res. Int. 2010, 43, 1803–1813. [Google Scholar] [CrossRef]
  154. Luo, J.; Tang, S.; Peng, X.; Yan, X.; Zeng, X.; Li, J.; Li, X.; Wu, G. Elucidation of cross-talk and specificity of early response mechanisms to salt and PEG simulated drought stresses in Brassica napus using comparative proteomic analysis. PLoS ONE 2015, 10, e0138974. [Google Scholar] [CrossRef] [PubMed]
  155. Timabud, T.; Yin, X.; Pongdontri, P.; Komatsu, S. Gel-free/label-free proteomic analysis of developing rice grains under heat stress. J. Proteomics 2016, 133, 1–19. [Google Scholar] [CrossRef] [PubMed]
  156. Qureshi, M.I.; Qadir, S.; Zolla, L. Proteomics-based dissection of stress-responsive pathways in plants. J. Plant Physiol. 2007, 164, 1239–1260. [Google Scholar] [CrossRef] [PubMed]
  157. Hao, P.; Zhu, J.; Gu, A.; Lv, D.; Ge, P.; Chen, G.; Li, X.; Yan, Y. An integrative proteome analysis of different seedling organs in tolerant and sensitive wheat cultivars under drought stress and recovery. Proteomics 2015, 15, 1544–1563. [Google Scholar] [CrossRef] [PubMed]
  158. Mirzaei, M.; Soltani, N.; Sarhadi, E.; Pascovici, D.; Keighley, T.; Salekdeh, G.H.; Haynes, P.A.; Atwell, B.J. Shotgun proteomic analysis of long-distance drought signaling in rice roots. J. Proteome Res. 2012, 11, 348–358. [Google Scholar] [CrossRef] [PubMed]
  159. Paul, S.; Gayen, D.; Datta, S.K.; Datta, K. Dissecting root proteome of transgenic rice cultivars unravels metabolic alterations and accumulation of novel stress responsive proteins under drought stress. Plant Sci. 2015, 234, 133–143. [Google Scholar] [CrossRef] [PubMed]
  160. Wang, N.; Zhao, J.; He, X.; Sun, H.; Zhang, G.; Wu, F. Comparative proteomic analysis of drought tolerance in the two contrasting Tibetan wild genotypes and cultivated genotype. BMC Genomics 2015, 16, 432. [Google Scholar] [CrossRef] [PubMed]
  161. Gil-Quintana, E.; Lyon, D.; Staudinger, C.; Wienkoop, S.; González, E.M. Medicago truncatula and Glycine max: Different drought tolerance and similar local response of the root nodule proteome. J. Proteome Res. 2015, 14, 5240–5251. [Google Scholar] [CrossRef] [PubMed]
  162. Han, F.; Chen, H.; Li, X.J.; Yang, M.F.; Liu, G.S.; Shen, S.H. A comparative proteomic analysis of rice seedlings under various high-temperature stresses. Biochim. Biophys. Acta 2009, 1794, 1625–1634. [Google Scholar] [CrossRef] [PubMed]
  163. Gupta, O.P.; Mishra, V.; Singh, N.K.; Tiwari, R.; Sharma, P.; Gupta, R.K.; Sharma, I. Deciphering the dynamics of changing proteins of tolerant and intolerant wheat seedlings subjected to heat stress. Mol. Biol. Rep. 2015, 42, 43–51. [Google Scholar] [CrossRef] [PubMed]
  164. Li, W.; Wei, Z.; Qiao, Z.; Wu, Z.; Cheng, L.; Wang, Y. Proteomics analysis of alfalfa response to heat stress. PLoS ONE 2013, 8, e82725. [Google Scholar] [CrossRef] [PubMed]
  165. Shakeel, S.N.; Aman, S.; Haq, N.U.; Heckathorn, S.A.; Luthe, D. Proteomic and transcriptomic analyses of Agave americana in response to heat stress. Plant Mol. Biol. Rep. 2013, 31, 840–851. [Google Scholar] [CrossRef]
  166. Jagadish, S.V.K.; Muthurajan, R.; Oane, R.; Wheeler, T.R.; Heuer, S.; Bennett, J.; Craufurd, P.Q. Physiological and proteomic approaches to address heat tolerance during anthesis in rice (Oryza sativa L.). J. Exp. Bot. 2010, 61, 143–156. [Google Scholar] [CrossRef] [PubMed]
  167. Shi, W.; Muthurajan, R.; Rahman, H.; Selvam, J.; Peng, S.; Zou, Y.; Jagadish, K.S.V. Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol. 2013, 197, 825–837. [Google Scholar] [CrossRef] [PubMed]
  168. Ren, C.; Bilyeu, K.D.; Beuselinck, P.R. Composition, vigor, and proteome of mature soybean seeds developed under high temperature. Crop Sci. 2009, 49, 1010–1022. [Google Scholar] [CrossRef]
  169. Hu, X.; Wu, L.; Zhao, F.; Zhang, D.; Li, N.; Zhu, G.; Li, C.; Wang, W. Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Front. Plant Sci. 2015, 6, 298. [Google Scholar] [CrossRef] [PubMed]
  170. Jagadish, S.V.K.; Muthurajan, R.; Rang, Z.W.; Malo, R.; Heuer, S.; Bennett, J.; Craufurd, P.Q. Spikelet proteomic response to combined water deficit and heat stress in rice (Oryza sativa cv. N22). Rice 2011, 4, 1–11. [Google Scholar] [CrossRef]
  171. Rollins, J.A.; Habte, E.; Templer, S.E.; Colby, T.; Schmidt, J.; von Korff, M. Leaf proteome alterations in the context of physiological and morphological responses to drought and heat stress in barley (Hordeum vulgare L.). J. Exp. Bot. 2013, 64, 3201–3212. [Google Scholar] [CrossRef] [PubMed]
  172. Hu, H.H.; Xiong, L.Z. Genetic engineering and breeding of drought-resistant crops. Annu. Rev. Plant Biol. 2014, 65, 715–741. [Google Scholar] [CrossRef] [PubMed]
  173. Araus, J.L.; Cairns, J.E. Field high-throughput phenotyping: The new crop breeding frontier. Trends Plant Sci. 2014, 19, 52–61. [Google Scholar] [CrossRef] [PubMed]
  174. Lynch, J.P.; Chimungu, J.G.; Brown, K.M. Root anatomical phenes associated with water acquisition from drying soil: Targets for crop improvement. J. Exp. Bot. 2014, 65, 6155–6166. [Google Scholar] [CrossRef] [PubMed]
  175. Dolferus, R. To grow or not to grow: A stressful decision for plants. Plant Sci. 2014, 229, 247–261. [Google Scholar] [CrossRef] [PubMed]
  176. Riesen, O.; Feller, U. Redistribution of nickel, cobalt, manganese, zinc, and cadmium via the phloem in young and maturing wheat. J. Plant Nutr. 2005, 28, 412–430. [Google Scholar] [CrossRef]
  177. Aharoni, A.; Dixit, S.; Jetter, R.; Thoenes, E.; van Arkel, G.; Pereira, A. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 2004, 16, 2463–2480. [Google Scholar] [CrossRef] [PubMed]
  178. Zhu, L.; Guo, J.; Zhu, J.S.; Zhou, C. Enhanced expression of EsWAX1 improves drought tolerance with increased accumulation of cuticular wax and ascorbic acid in transgenic Arabidopsis. Plant Physiol. Biochem. 2014, 75, 24–35. [Google Scholar] [CrossRef] [PubMed]
  179. Reynolds-Henne, C.E.; Langenegger, A.; Mani, J.; Schenk, N.; Zumsteg, A.; Feller, U. Interactions between temperature, drought and stomatal opening in legumes. Environ. Exp. Bot. 2010, 68, 37–43. [Google Scholar] [CrossRef]
  180. Gallé, A.; Feller, U. Changes of photosynthetic traits in beech saplings (Fagus sylvatica) under severe drought stress and during recovery. Physiol. Plant. 2007, 131, 412–421. [Google Scholar] [CrossRef] [PubMed]
  181. Stockey, R.A.; Ko, H. Cuticle micromorphology of Araucaria dejussieu. Bot. Gaz. 1986, 147, 508–548. [Google Scholar] [CrossRef]
  182. Lee, B.R.; Lee, D.G.; Avice, J.C.; Kim, T.H. Characterization of vegetative storage protein (VSP) and low molecular proteins induced by water deficit in stolon of white clover. Biochem. Biophys. Res. Commun. 2014, 443, 229–233. [Google Scholar] [CrossRef] [PubMed]
  183. Baloglu, M.C.; Eldem, V.; Hajyzadeh, M.; Unver, T. Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE 2014, 9, e96014. [Google Scholar] [CrossRef] [PubMed]
  184. Yan, H.R.; Jia, H.H.; Chen, X.B.; Hao, L.L.; An, H.L.; Guo, X.Q. The Cotton WRKY Transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol. 2014, 55, 2060–2076. [Google Scholar] [CrossRef] [PubMed]
  185. Yoshida, T.; Fujita, Y.; Maruyama, K.; Mogami, J.; Todaka, D.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 2015, 38, 35–49. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Schematic presentation of some key points for characterizing genotypes differing in drought tolerance. A: performance of non-stressed plants (pre-stress); B: performance under moderate drought; C: recovery from moderate drought; D: performance under severe drought; E: time course for recovery from severe drought; F: completeness of recovery from severe drought.
Figure 1. Schematic presentation of some key points for characterizing genotypes differing in drought tolerance. A: performance of non-stressed plants (pre-stress); B: performance under moderate drought; C: recovery from moderate drought; D: performance under severe drought; E: time course for recovery from severe drought; F: completeness of recovery from severe drought.
Agriculture 06 00026 g001 1024
Figure 2. Morphological and physiological characteristics of annual crops relevant for their responses to drought. A: rooting depth (before and during stress period); B: root branching; C: uptake of mineral nutrients and release to the shoot; D: interactions with mycorrhiza; E: nodulation and nodule activity (in legumes); F: production of abscisic acid (ABA) and release to the shoot; G: storage of nutrients and assimilates in roots/rhizomes/bulbs; H: transport of nutrients/assimilates/phytohormones via xylem and phloem; I: emergence and expansion of new leaves; J: production of new leaves from axillary buds; K: senescence of older leaves; L: number, size and morphological/physiological properties of mature leaves; M: spatial orientation, curling and wilting of mature leaves; N: maturation of fruits and seeds.
Figure 2. Morphological and physiological characteristics of annual crops relevant for their responses to drought. A: rooting depth (before and during stress period); B: root branching; C: uptake of mineral nutrients and release to the shoot; D: interactions with mycorrhiza; E: nodulation and nodule activity (in legumes); F: production of abscisic acid (ABA) and release to the shoot; G: storage of nutrients and assimilates in roots/rhizomes/bulbs; H: transport of nutrients/assimilates/phytohormones via xylem and phloem; I: emergence and expansion of new leaves; J: production of new leaves from axillary buds; K: senescence of older leaves; L: number, size and morphological/physiological properties of mature leaves; M: spatial orientation, curling and wilting of mature leaves; N: maturation of fruits and seeds.
Agriculture 06 00026 g002 1024
Figure 3. Morphological and physiological leaf characteristics relevant for the response to drought and heat. A: properties of the cuticle; B: deposition of epicuticular waxes; C: density, size and regulation of stomates; D: formation of stomatal plugs; E: mesophyll conductance; F: delivery of solutes via the xylem; G: metabolic properties of photosynthetically active cells; H: export of solutes via the phloem; I: deposition of vegetative storage proteins in the vacuoles of paraveinal mesophyll cells.
Figure 3. Morphological and physiological leaf characteristics relevant for the response to drought and heat. A: properties of the cuticle; B: deposition of epicuticular waxes; C: density, size and regulation of stomates; D: formation of stomatal plugs; E: mesophyll conductance; F: delivery of solutes via the xylem; G: metabolic properties of photosynthetically active cells; H: export of solutes via the phloem; I: deposition of vegetative storage proteins in the vacuoles of paraveinal mesophyll cells.
Agriculture 06 00026 g003 1024
Table 1. Leaf proteins involved in the responses to drought and/or heat.
Table 1. Leaf proteins involved in the responses to drought and/or heat.
ProteinProposed FunctionReferences
AquaporinsH2O transport through membranes[133]
DehydrinsStabilization of macromolecules[134,135,136]
Chaperonin-60 βStabilization of macromolecules[137]
Heat shock proteinsStabilization of cell constituents[138,139,140]
Cu/Zn Superoxide dismutaseDetoxification of reactive oxygen species[124,141]
Mn Superoxide dismutaseDetoxification of reactive oxygen species[124]
Fe Superoxide dismutaseDetoxification of reactive oxygen species[124]
Ascorbate peroxidaseDetoxification of reactive oxygen species[124,142]
CatalaseDetoxification of reactive oxygen species[124]
P5CS 1Accumulation of proline[143]
Rubisco activaseActivation of Rubisco (Calvin cycle)[6,144]
1 Delta-1-pyrroline-5-carboxylate synthetase (P5CS).
Table 2. Important traits involved in drought and/or heat responses of crop plants.
Table 2. Important traits involved in drought and/or heat responses of crop plants.
Trait Relevance for Abiotic Stress ResponseReferences
Rooting depthAccess to more suitable soil regions p,c[25,26,27,28,29]
Root branchingAccess to more suitable soil regions p,c[29,30,31,32,33,34,35,36,37]
Nutrient uptake into rootsAcquisition of mineral nutrients r,c[44,45,46,59]
Xylem loading in rootsTransfer of nutrients to the shoot r,c[57,58,59,60]
Nutrient assimilation in rootsAcquisition of mineral nutrients r,c[44,45,46]
MycorrhizationAcquisition of mineral nutrients/water r,c[56,61,62,63,64,65,66,67,68,69,70]
Nodulation in legumesSymbiotic nitrogen fixation p,c[76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95]
Storage functions in rootsStress survival and recovery p,c[13,52,53]
Release of nutrients to shootSupply of aerial parts with nutrients p,c[44,45,46]
Phytohormone release to shootRoot-to-shoot signaling r[47,48,49,50,51]
Root senescenceRoot architecture and functions p,c[43]
Xylem-to-phloem transferSolute channeling to leaves and fruits r[176]
Xylem embolism and repairAcropetal flux of water and solutes p[97,98,99]
Storage of reserves in the stemAccumulation of reserves for recovery r[104,105]
Shoot apical meristem activityShoot architecture and performance p,c[103]
Development of axillary budsShoot architecture and performance p,c[103]
Leaf expansion (final size)Shoot architecture and performance i,c[103]
Leaf orientationLight interception r[103]
Leaf senescenceLoss of assimilatory capacity i,c[103]
Leaf surface (wax deposition)Reduction of non-stomatal transpiration i[177,178]
Density and size of stomatesStomatal transpiration i[107,108,109,110]
Stomatal regulationReversible control of stomatal transpiration r[106,179]
Formation of stomatal plugReduction of stomatal transpiration i[180,181]
Mesophyll conductanceCO2 diffusion inside the leaf i[106]
Vegetative storage proteinsIntermediate storage of mobilized nitrogen r[182]
Intactness of organellesFunctionality of plastids and mitochondria p[26,112,113,114,115,116,117]
PhotosystemsLight energy conversion to ATP/NADPH r[132]
Rubisco activaseActivation of Rubisco (Calvin cycle) p,c[103,144]
Detoxification of ROSProtection of cell constituents/metabolism r[119,120,121,122,123,124,125,126,127,128,129,130,131,132]
Respiration in leavesMaintenance of basic cellular functions[9]
Compatible solutesProtection of cell constituents/metabolism r[143]
Transcription factorsRegulation of gene expression under stress r[183,184,185]
Dehydrin patternProtection of cell constituents r[134,135,136]
AquaporinsWater/CO2 transport across membranes p[133]
ChaperoninsProtection of enzymes r[137,138,139,140]
Cytokinin levels/effectsRegulation of metabolism and senescence r[48]
Proteolytic activitiesIntracellular protein degradation p,c[127]
Solute transport to fruitsYield formation p,c[145,146,147,148]
Seed maturation/compositionYield quantity and quality in seed crops p,c[5,160,168]
r reversible after stress period; p partially reversible; i irrversible; c can be compensated after stress phase.
Agriculture EISSN 2077-0472 Published by MDPI AG, Basel, Switzerland RSS E-Mail Table of Contents Alert
Back to Top