Next Article in Journal
Diversity of Endomycorrhizal Fungi in Argan Forest Stands: Implications for the Success of Reforestation Programs
Next Article in Special Issue
Effects of Shading on the Growth and Photosynthetic Fluorescence Characteristics of Castanopsis hystrix Seedlings of Top Community-Building Species in Southern Subtropical China
Previous Article in Journal
Genome-Wide Identification, Characterization, and Expression Profiling of the Glutaredoxin Gene Family in Tea Plant (Camellia sinensis)
Previous Article in Special Issue
Differences in Root Endophytic Bacterial Communities of Chinese Cork Oak (Quercus variabilis) Seedlings in Different Growth Years
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Forests
Volume 14
Issue 8
10.3390/f14081648
forests-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Adaptive Strategies Employed by Clonal Plants in Heterogeneous Patches

by
Pan Yang
1,2,†,
Li Huang
1,2,†,
Suni He
1,
Xianghua Zeng
1,
Yinyi Chen
1 and
Haimiao Wang
1,2,3,*
1
Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection, Guangxi Normal University, Ministry of Education, Guilin 541006, China
2
Guangxi Key Laboratory of Landscape Resources Conservation and Sustainable Utilization in Lijiang River Basin, Guangxi Normal University, Guilin 541006, China
3
College of Life Sciences, Guangxi Normal University, Guilin 541004, China
*
Author to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Forests 2023, 14(8), 1648; https://doi.org/10.3390/f14081648
Submission received: 22 May 2023 / Revised: 13 August 2023 / Accepted: 14 August 2023 / Published: 15 August 2023
(This article belongs to the Special Issue Adaptive Mechanisms of Tree Seedlings to Adapt to Stress)
Browse Figures
Review Reports Versions Notes

Abstract

:
Heterogeneity is widespread in natural environments; as a result, connected clonal ramets often live in areas characterized by patches of different resources. Specifically, clonal plants are frequently affected by conditions of heterogeneous water stress. This raises the question of how clonal plants grow and reproduce in areas with patches of different resources. In this study, we investigated the adaptation mechanisms of clonal plants under heterogeneous environmental conditions. On the one hand, we bore in mind that phenotypic plasticity is abundantly exhibited in clonal plants. Clonal plants respond to water stress mainly through regulation of the size of individuals, the allocation of population biomass, and the number of daughter plants, as well as the extension ability and branching intensity of clonal organs, which directly affect reproduction and population stability in clonal plants. On the other hand, we also considered the physiological integration in clonal plants which has been shown in many studies. Ramets of clonal plants normally stay connected to each other through horizontal connectors (stolons or rhizomes). Communicated substances and resources such as water, mineral nutrition, photosynthetic products, and secondary metabolites are translocated between ramets; by such means, the plant relieves stress caused by heterogeneous patches. In this study, we sought to obtain scientific references to improve our understanding of how clonal plants in natural environments acclimate to stresses caused by soil heterogeneity.

1. Introduction

Clonality in plants is widespread, including in species that span heterogeneous environments [1,2]. Such environments affect many essential functional traits and physiological processes in plants and also determine population structures and evolutionary processes [3]. Clonality is an important characteristic in clonal plants; clonal biological individuals have the ability to produce potentially independent offspring through vegetative reproduction [4,5,6]. Continuous vegetative reproduction promotes persistence when sexual reproduction is limited or absent, leading to higher population stability and ecosystem resilience [7]. As shown in Figure 1, a seedling that initially germinates from zygotes produced by the sexual reproduction process is termed the mother plant or the ortet. Individuals produced by clonal growth are called ramets, and these are capable of independent existence [8]. Clonal plants produce a number of genetically identical ramets that connect to each other by means of spacers; these are stolon or rhizome internodes which cover a physical distance for a period of time [9,10,11]. The length, branching intensity, and branching angles of spacers determine the placement pattern of clonal ramets in space [12]. A number of studies have shown that clonal plants exhibit a considerable degree of phenotypic plasticity in heterogeneous stress conditions, and that physiological integration is triggered so that the risks from stress habitats are shared [13,14,15,16]. Compared with non-clonal plants, clonal plants occupy larger areas of horizontal space by expanding into new habitats at an overwhelming rate, so that connected clonal ramets usually lie in different horizontal patches [3,17]. There are many ways to classify clonal plants. For example, they can be classified as root-derived, shoot-derived, or combined root-derived and shoot-derived types, according to the origin of clonal organs. A classification into two types can also be made based on the branching of clonal organs, so that there are monopodial-branching clonal plants and sympodial-branching clonal plants. Finally, depending upon the degree of dispersion of the ramets, clonal plants may also be classified as guerilla-growth, phalanx-growth, or intermediate-growth forms [3,18].
Clonal plants are widely distributed among ecosystems, and they dominate in different kinds of habitats, helping to maintain ecosystem balance [6,14]. A host of common economic plants, such as food crops, forage crops, and medicinal plants, exhibit clonal growth habits, as do many harmful weeds. Indeed, the benefits or harms of such plants are directly related to their clonal growth habits. In addition. recent studies have demonstrated that some clonal plants may be suitable for repairing and restoring vulnerable habitats. These include (a) clonal plants in karst landform habitats, such as Ficus tikoua [20], Alchornea trewioides [21], and Drepanostachyum luodianense [22]; (b) clonal plants in deserts, such as Calamagrostis epigejos [23], Hedysarum leave [24], Hippophae rhamnoides L., Psammochloa villosa [25], and Stenocereus eruca (Cactaceae) [26]; (c) clonal plants in grasslands, such as Leymus chinensis [27,28], Zoysia japonica Steud [29,30], and Buchloe dactyloides [31]; (d) clonal plants in wetlands, such as Phragmites australis [32,33], Paspalum paspaloides [34], Acorus calamus L., and Spartina alterniflora Loisel [34]. Researchers have also been keen to study the invasion mechanism in invasive clonal plants such as Alternanthera philoxeroides [35], Solidago canadensis L. [36], Carpobrotus edulis [37], and Mikania micrantha H.B.K. [38]. Studies such as those just mentioned have primarily focused on the unique characteristics of clonal growth, the structure of new ramet development, and the degree of physiological integration between ramets [39]. In brief, it may be said that the strategies employed by clonal plants to adapt to abiotic stress surroundings have been extensively studied by researchers [40]. However, the present published literature is lacking in overviews of adaptive strategies employed by clonal plants in response to heterogeneous water stresses.
In nature, spatial-temporal heterogeneity is very pervasive in resource distribution and plant habitat conditions [13,41]. Heterogeneous water stress is a habitat change that affects clonal plants frequently; indeed, it is the most prominent factor negatively influencing plant growth and development [42]. It has been reported that chronic or severe stress leads to low adaptability of plant populations to their environment [43] because physiological activities in individual plants are badly affected. The effects of water loss and the negative impacts of xylem sap pressures during drought have been mitigated by exploiting a variety of interdependent and coordinated morphological, anatomical, and physiological traits [44,45]. Drought eventually reduces the rate of photosynthesis by negatively impacting mesophyll conductance, Rubisco activity, and ATP synthase activity in leaves [46,47]. Many plants are able to accumulate ethylene rapidly after waterlogging, so ethylene content has been suggested as a reliable indicator of the waterlogging perception mechanism in plants [48]. It is known that, in most plants, leaf chlorophyll content decreases under flood conditions. This phenomenon may be readily explained. Waterlogging induces the synthesis of a large amount of ethylene, leading to up-regulation of chlorophyllase gene expression, enzyme activity, and the promotion of plant chlorophyll decomposition [49,50]. Under flood conditions, the carboxylation ability of Rubisco is far less than its oxygenation reaction; this explains the significant decrease in Rubisco carboxylase activity which has been found in many species of plant after waterlogging [51,52].
Positive interactions can alleviate the impact of abiotic stress upon plant communities and may also help counter the effects of climatic extremes [53]. In order to adapt to adverse environments, many plants are able to detect and respond to changes in soil moisture [31,54,55]. Plant roots can secrete root chemicals after sensing changes in soil habitats, and thus regulate water-use efficiency. Under water stress, more abscisic acid (ABA) is produced in roots and transported to leaves via the xylem; this regulates stomatal movement and thus affects water status and water balance in the plant [56]. The increase in ABA content helps to maintain the membrane structure and also plays a key role in acclimation memory in plants suffering drought stress. Because the plants retain a memory of the drought stress, the epigenome changes rapidly and produces physiological responses related to the new adaptive structure whenever non-fatal drought stress occurs again [57,58]. Studies have also shown that plants are often subjected to hypoxia during waterlogging; under such conditions, the core hypoxia genes are awakened, enabling recovery from prolonged hypoxia [59]. Some plant roots can develop more aeration tissues, such as adventitious roots, which partially compensate for root growth inhibition when waterlogging occurs [42]. Interactions among physiological integration, plant construction growth, and plastic responses have also been reported by researchers [9]; however, the adaptation mechanisms used by plants in heterogeneous water environments have not yet been systematically clarified. In this paper, therefore, we review the adaptation mechanisms (phenotypic plasticity and physiological integration among clonal ramets) under conditions of heterogeneous water stress, based on research on clonal plants published in the literature.

2. Phenotypic Plasticity of Clonal Plants in Response to Water Heterogeneity

In plants, plasticity is a persistent trait that affects the ability of plant populations to adapt to environmental changes [60,61,62]. In clonal plants, plasticity includes two aspects: clonal morphology and clonal growth. Phenotypic responses to a novel or extreme environment are initially plastic, with any genetic changes occurring only later. Some scholars have demonstrated that phenotypic plasticity is not a whole-plant response, but a property of individual meristems, leaves, branches, and roots, which is triggered by local environmental conditions [63]. In response to the stress caused by either excessive or scarce resources, the growing organs of clonal plants may exhibit changes in morphology, physiology, and biomass [64,65]; these can be seen as evolving traits targeted by natural selection. Clonal plants respond to water stress mainly through regulation of the size of individuals, the allocation of population biomass, and the number of daughter plants, as well as the extension ability and branching intensity of clonal organs, which directly affect reproduction and population stability in clonal plants [63,66,67,68]. In previous studies, the phenotypic plasticity of clonal plants under abiotic stress has been assessed using indexes such as the number and area of basal leaves, the number and density of clonal ramets, spacer length and specific spacer length, branching intensity and angle, and biomass [13]. Whether clonal plants benefit from the plasticity depends on the extent of phenotypic plasticity and the conditions of the growth environment.
Plasticity in resource uptake has been proven to be beneficial for plants in a wide range of environments [16]. Consequently, clonal plants can grow well in heterogeneous habitats, using ecological adaptation strategies for acquiring necessary resources formed during evolution [16]. So, what are the similarities and differences in the adaptation strategies of phenotypic plasticity in clonal plants when facing water heterogeneity? Compared with homogeneous water conditions, water heterogeneity exerts a greater influence on phenotypic plasticity in clonal plants. However, the ecological adaptation strategies of clonal plants are different in different habitats. These may be separately described as follows: (a) Clonal plants in sandy land. Ramets of Calamagrostis epigeios with optimal water supply condition were found to produce significantly more new rhizomes and more offspring (ramets), accumulate more shoot biomass, and allocate more biomass to their shoots, compared with those under a condition of insufficient water supply [23]. Clonal reproduction and the extension of clonal organs are therefore inhibited by heterogeneous water stress. (b) Clonal plants in grassland. When Zoysia japonica was subjected to heterogeneous water stress, the main stolon diameter of ramets was found to be significantly thicker in low water patches, but the growth and development of plants decreased significantly in high-water patches [69]. In another study, Calamagrostis pseudophragmites responded to water heterogeneity with increased growth of underground parts (rhizomes, roots, and buds) which promoted clonal reproduction and extension of clonal organs [17]. Because water heterogeneity is usually accompanied by heterogeneity of nutrients and other resources, the growth strategy of Calamagrostis pseudophragmites may be closely related to resource allocation. (c) Clonal plants in karst habitats. When Phyllostachys praecox was planted in a heterogeneous water environment, more substances were transported in the underground parts of the plant, and root biomass was significantly enhanced, so that the utilization rate of resources was increased. Contrarily, when soil water content was increased, substances tended to be used for the growth of ramets (overground part), while clonal rhizome lengths and root lengths decreased significantly [70]. Such morphological changes under conditions of water stress ensure higher competitiveness of clonal plants in light and air and enhance their dominance as species in a drought environment. (d) Invasive clonal plants that grow rapidly in many habitats. Clarifying the mechanism of biological invasion is a key step in predicting future invasion situations, and in mitigating the negative effects triggered by invasive clonal plants [37]. Many studies have demonstrated that clonal growth is an attribute of successful plant invasion [71,72]. The regeneration ability of small clonal fragments is also an important advantage of plant clonal growth. Furthermore, increased thickness of stolons and greater internode lengths can increase the survival rate of small-cloned fragments [38]. In one study, researchers found that the biomass of invasive species Carpobrotus Edulis (L.) increased after drought stress. Interestingly, this increase in biomass was mainly due to the production of above-ground structures which increased the spread along the soil surface, a finding with important implications for the likely success of this aggressive invader in colonizing new environments [37]. (e) Clonal plants of other habitats. Researchers found a positive correlation between the total biomass of Aegilops tauschii and soil moisture content. Any decrease in available moisture slows down growth and decreases the accumulation of biomass [67]. However, the ramets of Carex plants have been found to grow better in water-sufficient patches, as their roots grew longer [73]. It is beneficial for clonal plants to absorb as much water and nutrition as possible in areas of shallow soil. The adaptive strategies employed by plants from different habitats in response to heterogeneous water stress are summarized in Table 1.

3. Physiological Integration in Clonal Plants in Response to Water Heterogeneity

Physiological integration, as an important strategy used by clonal plants to adapt to their habitat, has been the subject of considerable attention by researchers. Physiological integration means that ramets of clonal plants normally stay connected through horizontal connectors (stolons or rhizomes). However, communication substances and resources have been shown to be translocated between ramets; these include water, mineral nutrition, photosynthetic products, and secondary metabolites [1,11,78]. For this paper, we designed a diagram to illustrate physiological responses in clonal plants under heterogeneous water stress, as shown in Figure 2. The source–sink relationship, water potential, and branch structure are primary factors determining clonal physiological integration [80,81,82]. Sharing of resources between ramets continues until young ramets are self-sufficient [83], and the transfer pattern of shared resources is related to growth season and tiller age [27]. The resource-sharing ability varies greatly between species and within species [84]. In general, if the total of resources in plants is limited, increased resource allocation to a specific organ may lead to reduced resource allocation for another organ [39,85]. For instance, the authors of one study found that investment in root production decreased while above-ground biomass increased under conditions of long-term water stress; this increase in biomass was mainly due to the production of above-ground structures, increasing the spread along the soil surface [37], with ramets transporting photosynthates to support their growth. In another study, it was shown that clonal integration promoted biomass partitioning both for apical ramets growing in conditions of low water availability and basal ramets growing in conditions of high-water availability [86]. This behavior provides the potential for rapid clonal growth when conditions improve; it also enhances the tolerance of clonal populations and increases the growth and reproduction of clonal plants [87,88,89,90].
Physiological integration alleviates the stress caused by water deficiency. Researchers have reported improved survival rates in water-stressed offspring ramets that remained connected to their parent plants [56,92]. Connected ramets have been shown to exhibit stronger resistance responses (e.g., higher antioxidant enzyme activity and proline content, lower O2− productivity, and MDA content) to induce resistance [74,93]. Photosynthesis is a physiological process in which plants are sensitive to environmental changes. Net photosynthetic rate (Pn), transpiration rate (Tr), and stomatal conductance (Gs) are the main parameters reflecting the photosynthetic capacity of plants [86]. The authors of [74] found that levels of chlorophyll content, the chlorophyll a/b ratio, and the photosynthetic parameters (Pn, Gs) of offspring ramets were not reduced when parents were subject to well-watered conditions and offspring ramets were under drought conditions [74]. These interesting results suggested that the physiological support provided by parent plants enables their offspring ramets to maintain high photosynthetic efficiencies. This itself demonstrates the benefits of physiological integration in terms of feedback regulation of photosynthesis. However, if the intensity of environmental stress or external interference reaches levels which exceed the individual’s tolerance and regulation ability, the risk of death to the basal plant cannot be overcome, and life in the basal plant is finally extinguished [94]. In recent years, to better study physiological integration in clonal plants, the isotope tracer method has been used as an accurate direct method [82] while cutting off roots and stems, defoliation, and shading are indirect methods that have also been widely used [10,24,31,95]. The adaptations of some clonal plants to conditions of water heterogeneity by means of physiological integration—and the specific research methods used to investigate this adaptation—are summarized in Table 2.

4. Conclusions

In clonal plants, physiological responses to drought or waterlogging are characterized by regulation of the endogenous protective enzyme system, endogenous hormone level, and carbohydrate metabolism. This can be understood as an adaptation to habitat stress. ABA content increases when water is deficient, regulating stomatal movement, and leading to a decrease in carbon dioxide content; this results in an energy surplus, which leads to photooxidative stress and causes antioxidant defense of the plant organism. Moreover, drought can result in lower levels of chlorophyll content; this slows down photosynthesis and triggers resistance to drought as a short-term stress condition. In addition, the activity of endogenous protective enzymes increases, helping to inhibit the accumulation of reactive oxygen species (ROS), and thereby enhancing the drought tolerance of the plant organism. Under conditions of waterlogging, Ca2+ and ROS signal pathways are awakened, and the formation of aerenchyma is also induced. Furthermore, the activities of SOD, APX, GPX, GST, CAT, and other enzymes all increase; however, respiration and ATP production decrease, sucrose and starch metabolism in tissues is regulated, and the ability to resist drought or waterlogging stress is triggered (Figure 3). Water heterogeneity is widespread in natural environments and exerts profound effects on growth and reproduction in plants, especially clonal plants. Under heterogeneous conditions, physiological integration in clonal plants may be triggered by a series of reactions, including responses to water reallocation and photosynthetic products. Finally, corresponding changes in morphology also occur, and these can be understood as a survival countermeasure in adapting to heterogeneous stress conditions. In short, this review provides a theoretical basis for understanding the adaptive mechanism in clonal plants to conditions of heterogeneity in natural environments.

Author Contributions

P.Y., L.H. and H.W. wrote the paper; S.H., X.Z. and Y.C. produced the figures and tables. All the authors contributed to the editing and revision of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

We appreciate the financial support from the Special Program for Technology Bases and Talents of Guangxi (2022AC20002), the Innovation-driven Development Project of Guangxi (AA20161002), the Innovation Project of Guangxi Graduate Education (JGY2023050), and the Sustainable Development Innovation and Key Program of Guangxi Normal University (2018ZD005, 2020CX004). We are also grateful for the Research Funds of the Guangxi Key Laboratory of Landscape Resources Conservation and Sustainable Utilization in Lijiang River Basin (LRCSU21Z0317) and the Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, China.

Data Availability Statement

The original contributions presented in the study are included in the article; further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Cornelissen, J.H.C.; Song, Y.; Yu, F.; Dong, M. Plant traits and ecosystem effects of clonality: A new research agenda. Ann. Bot. 2014, 114, 369–376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  2. Douhovnikoff, V.; Dodd, R.S. Epigenetics: A potential mechanism for clonal plant success. Plant Ecol. 2015, 216, 227–233. [Google Scholar] [CrossRef]
  3. Klimeová, J.; Ottaviani, G.; Charles-Dominique, T.; Campetella, G.; Canullo, R.; Chelli, S.; Janovský, Z.; Lubbe, F.C.; Martínková, J.; Herben, T. Incorporating clonality into the plant ecology research agenda. Trends Plant Sci. 2021, 12, 1237–1247. [Google Scholar] [CrossRef] [PubMed]
  4. Hong, R.; Wang, Y.; Huang, D. Introduction to clonal genetics of plant populations-the task, nature, origin and development. Acta Ecol. Sin. 2004, 24, 865–867. [Google Scholar]
  5. Dong, M.; Yu, F.; Alpert, P. Ecological consequences of plant clonality preface. Ann. Bot. 2014, 114, 367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Liu, F.; Liu, J.; Dong, M. ; Liu, J.; Dong, M. Ecological consequences of clonal integration in plants. Front. Plant Sci. 2016, 7, 770–781. [Google Scholar]
  7. Witte, L.C.; Stöcklin, J. Longevity of clonal plants: Why it matters and how to measure it. Ann. Bot. 2010, 106, 859–870. [Google Scholar] [CrossRef]
  8. Eriksson, O. Dynamics of genets in clonal plants. Trends Ecol. Evol. 1993, 8, 313–316. [Google Scholar] [CrossRef]
  9. Oborny, B.; Mony, C.; Herben, T. From virtual plants to real communities: A review of modelling clonal growth. Mol. Ecol. 2012, 234, 3–19. [Google Scholar] [CrossRef]
  10. Li, Y.; Chen, J.; Xue, G.; Peng, Y.; Song, H. Effect of clonal integration on nitrogen cycling in rhizosphere of rhizomatous clonal plant, Phyllostachys bissetii, under heterogeneous light. Sci. Total Environ. 2018, 628, 594–602. [Google Scholar] [CrossRef]
  11. Bittebiere, A.K.; Benot, M.L.; Mony, C. Clonality as a key but overlooked driver of biotic interactions in plants. Perspect. Plant Ecol. 2020, 43, 125510. [Google Scholar] [CrossRef]
  12. Chen, D.; Ali, A.; Yong, X.; Lin, C.; Niu, X.; Cai, A.; Dong, B.; Zhou, Z.; Wang, Y.; Yu, F. A multi-species comparison of selective placement patterns of ramets in invasive alien and native clonal plants to light, soil nutrient and water heterogeneity. Sci. Total Environ. 2019, 657, 1568–1577. [Google Scholar] [CrossRef]
  13. Dong, M. Plant clone growth in heterogeneous habitats: Risk spreading. Acta Phytoecol. Sin. 1996, 20, 543–548. [Google Scholar]
  14. Dong, M. Clonal growth in plants in relation to resource heterogeneity foraging behavior. Acta Bot. Sin. 1996, 38, 828–835. [Google Scholar]
  15. Chen, Y.; Dong, M. Relative importance of clonal and non-clonal plants in the landscape dynamics of Mu us Sandy land. Acta Phytoecol. Sin. 2002, 26, 377–380. [Google Scholar]
  16. Magyar, G.; Kun, Á.; Oborny, B.; Stuefer, J.F. Importance of plasticity and decision-making strategies for plant resource acquisition in spatio-temporally variable environments. New Phytol. 2007, 174, 182–193. [Google Scholar] [CrossRef]
  17. Ye, X.; Hu, Y.; Liu, Z.; Gao, S.; Dong, M. Water heterogeneous affects water storage in two rhizomatous clonal plants Leymus secalinus and Calamagrostis pseudophragmites. Acta Phytoecol. Sin. 2013, 37, 427–435. [Google Scholar]
  18. Klime, L.; Klimeová, J.; Hendriks, R.; van Groenendael, J. Clonal plant architecture: A comparative analysis of form and function. In The Ecology and Evolution of Clonal Plants, 2nd ed.; Kroon, H., Groenendael, J., Eds.; Backhuys Publishers: Leiden, The Netherlands, 1997; Volume 3, pp. 1–29. [Google Scholar]
  19. Zhou, J.; Mei, J.; Ma, J.; Zhang, Y.; Wang, H.; Jian, R. Characteristics of clonal reproduction of Alchornea trewioides in karst region of Guilin, China. J. Guangxi Norm. Univ. 2020, 38, 110–116. [Google Scholar]
  20. Liu, C.; Liu, Y.; Guo, K.; Fan, D.; Yu, L.; Yang, R. Exploitation of patchy soil water resources by the clonal vine Ficus tikoua in karst habitats of southwestern China. Acta Physiol. Plant. 2011, 33, 93–102. [Google Scholar] [CrossRef]
  21. Nie, Y.; Chen, H.; Wang, K.; Tan, W.; Deng, P.; Yang, J. Seasonal water use patterns of woody species growing on the continuous dolostone outcrops and nearby thin soils in subtropical China. Plant Soil 2011, 341, 399–412. [Google Scholar] [CrossRef]
  22. Liu, J.; Liao, X.; Zhang, D.; Wang, M.; Zhao, X. Population characteristics of Drepanostachyum ludianense in karst area of Guizhou, China. J. Pure Appl. Microbiol. 2014, 8, 2755–2760. [Google Scholar]
  23. Zhang, C.; Yu, F.; Chen, Y.; Dong, M. Phenotypic plasticity in response to the heterogeneous water supply in the rhizomatous grass species, Calamagrostis epigejos in the Mu Us Sandy Land of China. Acta Bot. Sin. 2003, 45, 1210–1217. [Google Scholar]
  24. Zhang, C.; Yang, C.; Dong, M. The clonal integration of photosynthates in the rhizomatous half-shrub Hedysarum laeve. Acta Ecol. Sin. 2001, 12, 1986–1993. [Google Scholar]
  25. Yu, F.; Dong, M.; Bertil, K. Clonal integration helps Psammochloa villosa survive sand burial in an inland dune. New Phytol. 2004, 162, 697–704. [Google Scholar] [CrossRef]
  26. Ricardo, C.T.; Cecilia, A.C.; Luis, E.E.; Francisco, M.F. Clonal diversity and distribution in Stenocereus eruca (Cactaceae), a narrow endemic cactus of the Sonoran Desert. Am. J. Bot. 2005, 92, 272–278. [Google Scholar]
  27. Wang, Y.; Hong, R.; Huang, D.; Teng, X.; Li, Y.; Masae, S.; Miki, N. The translocation of photosynthate between clonal ramets of Leymus chinensis population. Acta Ecol. Sin. 2004, 17, 3097–3109. [Google Scholar]
  28. Abdullah, I. Study on Restoration of Saline Alkali Patchy Degraded Grassland Based on Spatial Expansion of Dominant Clonal Grass- Leymus chinensis in Songnen Grassland of Northeast China. Ph.D. Thesis, Northeast Normal University, Changchun, China, 2020. [Google Scholar]
  29. Cheng, L.; Li, D.; Zhu, Z.; Wang, H.; Ji, Q.; Li, W.; Chen, H.; Lai, S. Analysis on the characteristics of water physiological integration pattern and the ecological effects in clonal plant species Zoysia japonica. Acta Bot. Boreal. Sin. 2013, 33, 1442–1451. [Google Scholar]
  30. Xu, S.; Liu, Y.; Li, H.; Chen, Z.; Li, Y.; Zhang, L. Physiological integration of growth, carbohydrates, and soluble protein of Zoysia japonica clonal ramets under nutrient heterogeneity. Chin. J. Appl. Ecol. 2018, 29, 3569–3576. [Google Scholar]
  31. Qian, Y.; Li, D.; Han, L.; Sun, Z. Inter-ramet photosynthate translocation in Buffalograss under differential water deficit stress. J. Am. Soc. Hortic. Sci. 2010, 135, 310–316. [Google Scholar] [CrossRef] [Green Version]
  32. Kirk, H.; Paul, J.; Straka, J.; Freeland, J. Long-distance dispersal and high genetic diversity are implicated in the invasive spread of the common reed, Phragmites australis (Poaceae), in northeastern North America. Am. J. Bot. 2011, 98, 1180–1190. [Google Scholar] [CrossRef]
  33. Jiao, L.; Li, F.; Liu, X.; Wang, S.; Zhou, Y. Fine-Scale distribution patterns of Phragmites australis populations across an environmental gradient in the salt marsh wetland of dunhuang, China. Sustainability 2020, 12, 1671. [Google Scholar] [CrossRef] [Green Version]
  34. Yu, H.; Wang, L.; Liu, C.; Yu, D.; Qu, J. Effects of a spatially heterogeneous nutrient distribution on the growth of clonal wetland plants. BMC Ecol. 2020, 20, 59. [Google Scholar] [CrossRef]
  35. Wang, N.; Yu, F.; Li, P.; He, W.; Liu, F.; Liu, J.; Dong, M. Clonal integration affects growth, photosynthetic efficiency and biomass allocation, but not the competitive ability, of the alien invasive Alternanthera philoxeroides under severe stress. Ann. Bot. 2008, 101, 671–678. [Google Scholar] [CrossRef]
  36. Szymura, M.; Szymura, T. Growth, phenology, and biomass allocation of alien Solidago species in central Europe. Plant Spec. Biol. 2015, 30, 245–256. [Google Scholar] [CrossRef]
  37. Yaiza, L.L.; Marta, S.R.; Sergio, R.R.; Luís, G. Clonal integration facilitates the colonization of drought environments by plant invaders. AoB Plants 2016, 8, plw023. [Google Scholar]
  38. Huang, Q.; Shen, Y.; Li, X.; Zhang, G.; Huang, D.; Fan, Z. Regeneration capacity of the small clonal fragments of the invasive Mikania micrantha H.B.K.: Effects of the stolon thickness, internode length and presence of leaves. Weed Biol. Manag. 2015, 15, 70–77. [Google Scholar] [CrossRef]
  39. Weiner, J. Allocation, plasticity and allometry in plants. Perspect. Plant Ecol. 2004, 6, 207–215. [Google Scholar] [CrossRef]
  40. Semchenko, M.; John, E.A.; Hutchings, M.J. Effects of physical connection and genetic identity of neighbouring ramets on root-placement patterns in two clonal species. New Phytol. 2007, 176, 644–654. [Google Scholar] [CrossRef]
  41. Hutchings, M.J.; Wijesinghe, D.K. Patchy habitats, division of labour and growth dividends in clonal plants. Trends Ecol. Evol. 1997, 12, 320–325. [Google Scholar] [CrossRef]
  42. Yamauchi, T.; Colmer, T.D.; Pedersen, O.; Nakazono, M.; Notes, A. Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress. Plant Physiol. 2018, 176, 1118–1130. [Google Scholar] [CrossRef] [Green Version]
  43. Zhang, Y.; Zhang, Q.; Sammul, M. Physiological integration ameliorates negative efects of drought stress in the clonal herb Fragaria orientalis. PLoS ONE 2012, 7, e44221. [Google Scholar]
  44. Choat, B.; Brodribb, T.J.; Brodersen, C.R.; Duursma, R.A.; López, R.; Medlyn, B.E. Triggers of tree mortality under drought. Nature 2018, 558, 531–539. [Google Scholar] [CrossRef] [PubMed]
  45. Brodribb, T.J.; Powers, J.; Cochard, H.; Choat, B. Hanging by a thread? forests and drought. Science 2020, 368, 261–266. [Google Scholar] [CrossRef] [PubMed]
  46. Flexas, J.; Bota, J.; Loreto, F.; Cornic, G.; Sharkey, T.D. Diffusive and metabolic limitations to photosynthesis under drought and salinity in C3 plants. Plant Biol. 2004, 6, 269–279. [Google Scholar] [CrossRef]
  47. Carmo-Silva, A.E.; Gore, M.A.; Andrade-Sanchez, P.; French, A.N.; Hunsaker, D.J.; Salvucci, M.E. Decreased CO2 availability and inactivation of Rubisco limit photosynthesis in cotton plants under heat and drought stress in the field. Environ. Exp. Bot. 2012, 83, 1–11. [Google Scholar] [CrossRef]
  48. Sasidharan, R.; Hartman, S.; Liu, Z.; Martopawiro, S.; Sajeev, N.; van Veen, H.; Yeung, E.; Voesenek, L.A.C.J. Signal dynamics and interactions during flooding stress. Plant Physiol. 2018, 176, 1106–1117. [Google Scholar] [CrossRef] [Green Version]
  49. Sarkar, R.K.; Das, S.; Ravi, I. Changes in certain antioxidative enzymes and growth parameters as a result of complete submergence and subsequent re-aeration of rice cultivars differing in submergence tolerance. J. Agron. Crop Sci. 2001, 187, 69–74. [Google Scholar] [CrossRef]
  50. Ella, E.S.; Kawano, N.; Yamauchi, Y.; Tanaka, K.; Ismail, A.M. Blocking ethylene perception enhances flooding tolerance in rice seedlings. Funct. Plant Biol. 2003, 30, 813–819. [Google Scholar] [CrossRef]
  51. Cristina, B.; Kayla, K.; Charles, J.; Cynthia, L.; Julia, B. Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J. 2008, 56, 743–755. [Google Scholar]
  52. Narsai, R.; Rocha, M.; Geigenberger, P.; Whelan, J.; Dongen, J.T. Comparative analysis between plant species of transcriptional and metabolic responses to hypoxia. New Phytol. 2011, 190, 472–487. [Google Scholar] [CrossRef]
  53. Filazzola, A.; Liczner, A.R.; Westphal, M.; Lortie, C.J. The effect of consumer pressure and abiotic stress on positive plant interactions are mediated by extreme climatic events. New Phytol. 2018, 217, 140–150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Fabregas, N.; Fernie, A.R. The metabolic response to drought. J. Exp. Bot. 2019, 70, 1077–1085. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Jing, X.; Cai, C.; Fan, S.; Liu, C.; Wu, C.; Chen, B. Effects of rhizome integration on the water physiology of Phyllostachys edulis clones under heterogeneous water stress. Plants 2020, 9, 373. [Google Scholar] [CrossRef] [Green Version]
  56. Mao, S.; Jiang, C.; Zhang, W.; Zhang, J.; Chow, W.S.; Yang, J. Water translocation between ramets of strawberry during soil drying and its effects on photosynthetic performance. Physiol. Plant. 2009, 137, 225–234. [Google Scholar] [CrossRef]
  57. Eva, F.S.; Sergi, M.B. Stress memory and the inevitable effects of drought: A physiological perspective. Front. Plant Sci. 2016, 7, 1–6. [Google Scholar]
  58. Li, X.; Jimoh, S.O.; Li, Y.; Duan, J.; Cui, Y.; Jin, K.; Wang, Z.; Zhang, Y. Stress memory and phyllosphere/soil legacy underlie tolerance and plasticity of Leymus chinensis to periodic drought risk. Agric. For. Meteorol. 2022, 312, 108717. [Google Scholar] [CrossRef]
  59. Hartman, S.; Sasidharan, R.; Voesenek, L.A.C.J. The role of ethylene in metabolic acclimations to low oxygen. New Phytol. 2020, 229, 64–70. [Google Scholar] [CrossRef] [PubMed]
  60. Puijalon, S.; Bouma, T.J.; Van Groenendael, J.; Bornette, G. Clonal plasticity of aquatic plant species submitted to mechanical stress: Escape versus resistance strategy. Ann. Bot. 2008, 102, 989–996. [Google Scholar] [CrossRef] [Green Version]
  61. Radersma, R.; Noble, D.; Uller, T. Plasticity leaves a phenotypic signature during local adaptation. Evol. Lett. 2020, 4, 360–370. [Google Scholar] [CrossRef]
  62. Matesanz, S.; Mario, B.S.; Ramos-Muoz, M.; Cruz, M.D.L.; Benavides, R.; Adrián, E. Phenotypic integration does not constrain phenotypic plasticity: Differential plasticity of traits is associated to their integration across environments. New Phytol. 2021, 231, 2359–2370. [Google Scholar] [CrossRef]
  63. deKroon, H.; Huber, H.; Stuefer, J.F.; van Groenendael, J.M. A modular concept of phenotypic plasticity in plants. New Phytol. 2005, 166, 73–82. [Google Scholar] [CrossRef] [PubMed]
  64. Pauls, S.U.; Nowak, C.; Ba’lint, M.; Pfenninger, M. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 2013, 22, 925–946. [Google Scholar] [CrossRef]
  65. Bufford, J.L.; Hulme, P.E. Increased adaptive phenotypic plasticity in the introduced range in alien weeds under drought and flooding. Biol. Invasions 2021, 23, 2675–2688. [Google Scholar] [CrossRef]
  66. Li, L.; Geng, Y.; Lan, Z.; Cheng, J.; Song, Z. Phenotypic plasticity of aquatic plants in heterogeneous environments: A review. Biodivers. Sci. 2016, 24, 216–227. [Google Scholar] [CrossRef]
  67. Wang, N.; Chen, H.; Dong, Y.; Yuan, M. Effects of soil-water conditions on phological plasticity and allelopathic potential of invasive plant Aegilops tauschii Coss. Acta Agrestia Sin. 2018, 26, 402–408. [Google Scholar]
  68. Freschet, G.T.; Cyrille, V.; Bourget, M.Y.; Michael, S.L.; Florian, F. Allocation, morphology, physiology, architecture: The multiple facets of plant above- and below-ground responses to resource stress. New Phytol. 2018, 219, 1338–1352. [Google Scholar] [CrossRef]
  69. Zhu, Z. Effect of different soil moisture and severing stolon on clonal plasticity in Zoysia japonica steud a clonal plant. J. Anhui Agric. Sci. 2010, 38, 18627–18630. [Google Scholar]
  70. Yue, C.; He, Q.; Wang, K.; Weng, F. Growth of Phyllostachys praecox cv. prevernalis clone in different conditions of soil moisture. J. Zhejiang For. Sci. Technol. 2002, 22, 25–27. [Google Scholar]
  71. Yu, F.; Roiloa, S.R.; Peter, A. Global change, clonal growth, and biological invasions by plants. Front. Plant Sci. 2016, 7, 1467. [Google Scholar] [CrossRef] [Green Version]
  72. Huang, Q.; Li, X.; Huang, F.; Wang, R.; Lu, B.; Shen, Y.; Fan, Z.; Lin, P. Nutrient addition increases the capacity for division of labor and the benefits of clonal integration in an invasive plant. Sci. Total Environ. 2018, 643, 1232–1238. [Google Scholar] [CrossRef]
  73. deKroon, H.; Fransen, B.; van Rheenen, J.W.A.; van Dijk, A.; Kreulen, R. High levels of inter-ramet water translocation in two rhizomatous Carex species, as quantified by deuterium labelling. Oecologia 1996, 106, 73–84. [Google Scholar] [CrossRef] [PubMed]
  74. Li, Y.; Ning, W.; Xu, S.; Yu, N.; Chen, Z.; Zhang, L. Response of physiological integration in the clonal herb Zoysia japonica to heterogeneous water conditions. Acta Physiol. Plant 2022, 44, 34. [Google Scholar] [CrossRef]
  75. Wang, J.; Song, H.; Cheng, J.; Zhang, J.; Li, S.; Tao, J.; Liu, J. Respose strategies of Lolium perenne L. to karst heterogeneous habitats under drought stress. Acta Ecol. Sin. 2020, 40, 4566–4572. [Google Scholar]
  76. Liu, J.; Li, P.; Liao, X.; Zhao, X.; Wen, P.; Chi, X.; Yan, Q. Effect of drought stress on physiological and biochemical characteristics in Drepanostachyum luodianense. Acta Agric. Boreal. Sin. 2013, 22, 153–157. [Google Scholar]
  77. Peng, Y.; Luo, L.; Li, H.; Yu, F. Growth responses of a rhizomatous herb Bolboschoenus planiculmis to scale and contrast of soil nutrient heterogeneity. Chin. J. Plant Ecol. 2013, 37, 335–343. [Google Scholar] [CrossRef]
  78. Dong, B.; Alpert, P.; Zhang, Q.; Yu, F. Clonal integration in homogeneous environments increases performance of Alternanthera philoxeroides. Oecologia 2015, 179, 393–403. [Google Scholar] [CrossRef]
  79. Ge, J.; He, J.; Sun, X.; Chen, Q. Ecological responses of the invasive alien plant Solidago canadensis to changes of soil water content. Acta Bot. Boreal. Sin. 2010, 30, 575–585. [Google Scholar]
  80. Chapman, D.F.; Robson, M.J.; Snaydon, R.W. Physiological integration in the clonal perennial herb Trifolium repens L. Oecologia 1992, 89, 338–347. [Google Scholar] [CrossRef]
  81. Roiloa, S.R.; Retuerto, R. Responses of the clonal Fragaria vesca to microtopographic heterogeneity under different water and light conditions. Environ. Exp. Bot. 2007, 61, 1–9. [Google Scholar] [CrossRef]
  82. Shi, J.; Mao, S.; Wang, L.; Ye, X.; Wu, J.; Wang, G.; Chen, F.; Yang, Q. Clonal integration driven by source-sink relationships is constrained by rhizome branching architecture in a running bamboo species (Phyllostachys glauca): A 15N assessment in the field. For. Ecol. Manag. 2021, 481, 1–9. [Google Scholar] [CrossRef]
  83. Jaafry, S.; Li, D.; Chen, H.; Niu, X.; Li, B. Relative costs and benefits of clonal integration of Zoysia japonica under various N:P ratios. Nord. J. Bot. 2018, 36, njb-01795. [Google Scholar] [CrossRef] [Green Version]
  84. Wang, Y.; Müller-Schärer, H.; van Kleunen, M.; Cai, A.; Zhang, P.; Yan, R.; Dong, B.; Yu, F. Invasive alien plants benefit more from clonal integration in heterogeneous environments than natives. New Phytol. 2017, 216, 1072–1078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  85. Weiner, J.; Campbell, L.G.; Pino, J.; Echarte, L. The allometry of reproduction within plant populations. J. Ecol. 2009, 97, 1220–1233. [Google Scholar] [CrossRef]
  86. Wei, Q.; Li, Q.; Jin, Y.; Li, K.; Lei, N.; Chen, J. Effects of clonal integration on photochemical activity and growth performance of stoloniferous herb Centella asiatica suffering from heterogeneous water availability. Flora 2019, 256, 36–42. [Google Scholar] [CrossRef]
  87. Slade, A.J.; Hutchings, A. An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb glechoma hederacea. Oecologia 1987, 73, 425–431. [Google Scholar] [CrossRef] [PubMed]
  88. Gross, K.L.; Pregitzer, K.S.; Burton, A.J. Spatial variation in nitrogen availability in three successional plant communities. J. Ecol. 1995, 83, 357–367. [Google Scholar] [CrossRef]
  89. Yu, F.H.; Wang, N.; He, W.M.; Chu, Y.; Dong, M. Adaptation of rhizome connections in drylands: Increasing tolerance of clones to wind erosion. Ann. Bot. 2008, 102, 571–577. [Google Scholar] [CrossRef] [Green Version]
  90. Wang, P.; Alpert, P.; Yu, F. Clonal integration increases relative competitive ability in an invasive aquatic plant. Am. J. Bot. 2016, 103, 2079–2086. [Google Scholar] [CrossRef] [Green Version]
  91. Liu, L.; Zuo, S.; Ma, M.; Li, J.; Guo, L.; Huang, D. Appropriate nitrogen addition regulates reproductive strategies of Leymus chinensis. Glob. Ecol. Conserv. 2021, 27, e01599. [Google Scholar] [CrossRef]
  92. Roiloa, S.R.; Antelo, B.; Retuerto, R. Physiological integration modifiesd 15N in the clonal plant Fragaria vesca, suggesting preferential transport of nitrogen to water-stressed offspring. Ann. Bot. 2014, 114, 399–411. [Google Scholar] [CrossRef] [Green Version]
  93. Wei, Q.; Li, Q.; Jin, Y.; Wu, S.; Fan, L.; Lei, N.; Chen, J. Transportation or sharing of stress signals among interconnected ramets improves systemic resistance of clonal networks to water stress. Funct. Plant Biol. 2019, 46, 613–623. [Google Scholar] [CrossRef]
  94. Chen, J.; Dong, M.; Yu, D. Intraclonal spatial division of labour in two stoloniferous plants with different branching type in response to reciprocal patchiness of resources. Acta Ecol. Sin. 2004, 24, 921–924. [Google Scholar]
  95. Emmanuel, A.K.; Annie, D.R.; Francine, T. Physiological integration of connected balsam poplar ramets. Tree Physiol. 2016, 7, 797–806. [Google Scholar]
  96. Zhu, C.; Li, W.; Chen, Y.; Chen, Y. Characteristics of water physiological integration and its ecological significance for Populus euphratica young ramets in an extremely drought environment. J. Geophys. Res. 2018, 123, 5657–5666. [Google Scholar] [CrossRef]
  97. Luo, D.; Qian, Y.; Liu, J.; Han, L.; Sun, Z. Phenotypic responses of a clonal plant (Buchloe dactyloides) to nutrient heterogeneity. Acta Pratacul. Sin. 2014, 23, 104–109. [Google Scholar]
  98. Xiang, Y.; Zhang, F.; Duan, J.; Huang, H.; He, D.; Liu, Y.; Tao, J. Effects of clonal integration on biomass allocation and leaf structure of Glechoma longituba (Nakai) kupr in different water availability. Bull. Bot. Res. 2019, 39, 200–207. [Google Scholar]
  99. Hutchings, M.J.; Price, E.A.C. The causes and developmental effects of integration and independence between different parts of Glechoma hederacea clones. Oikos 2019, 63, 376–386. [Google Scholar]
Forests 14 01648 g001
Figure 1. A diagram of clonal plants [19].
Figure 1. A diagram of clonal plants [19].
Forests 14 01648 g001
Forests 14 01648 g002
Figure 2. Adaptive strategies of clonal plants under heterogeneous water stress [91].
Figure 2. Adaptive strategies of clonal plants under heterogeneous water stress [91].
Forests 14 01648 g002
Forests 14 01648 g003
Figure 3. Physiological integration to enhance adaptation to heterogeneous water stress in clonal plants. ROS—reactive oxygen species; SOD—superoxide dismutase; APX—ascorbate peroxidase; GPX—glutathione peroxidase; GST—glutathione s-transferase; CAT—catalase.
Figure 3. Physiological integration to enhance adaptation to heterogeneous water stress in clonal plants. ROS—reactive oxygen species; SOD—superoxide dismutase; APX—ascorbate peroxidase; GPX—glutathione peroxidase; GST—glutathione s-transferase; CAT—catalase.
Forests 14 01648 g003
Table 1. Adaptive strategies of clonal plants from different habitats under heterogeneous water stress.
Table 1. Adaptive strategies of clonal plants from different habitats under heterogeneous water stress.
CategoryPlantGrowth Form (Guerilla/Phalanx/Intermediate)Adaptation MechanismRef.
Desert clonal plantCalamagrostis epigejosGuerillaThe growth characteristics of ramet rhizome, the number of new ramets, and biomass allocation were all changed.[23]
Grassland clonal plantZoysia japonicaGuerillaContent levels of CAT (catalase), proline, and MDA (malondialdehyde) were significantly increased.[74]
Karst clonal plantLolium perenne L.PhalanxThe plant responded to stress by increasing specific root length and specific root area in deep-soil areas, and by reducing root tissue density.[75]
Drepanostachyum luodianensePhalanxThe degree of membrane lipid peroxidation was reduced by increasing the content of osmotic adjustment substances, and by increasing coordination between protective enzymes.[76]
Wetland clonal plantTypha orientalisGuerrillaPlant height, number of ramets, interval diameter and length, and biomass accumulation were significantly increased.[34]
Bolboschoenus planiculmisIntermediatePlant biomass, rhizome length, bulb number, total leaf length, plant height, spacer length, and root–shoot ratio were changed.[77]
Other clonal plantAlternanthera philoxeroidesGuerrillaMaximum quantum yield of photosystem II, total biomass, ramet number, and total stolon length were significantly reduced.[78]
Solidago canadensis L.GuerrillaGrowth, biomass allocation, clonal characteristics, and photosynthetic physiology were regulated.[79]
Table 2. Physiological response of physiological integration in some clonal plants under water heterogeneity.
Table 2. Physiological response of physiological integration in some clonal plants under water heterogeneity.
SpeciesTree/
Shrub/Herb		Research MethodsIntegrated SubstanceTransport DirectionIntegration ResultRef.
Populus euphraticaTreeSap flow monitoringWaterAcopetalThere was a cost tradeoff in the water physiology integration of offspring ramets.[96]
Populus balsamifera L.TreeConnecting/severing stemWater Net photosynthesis, stomatal conductance, and leaf water potential of stressed ramets were not affected by water exchange.[94]
Hedysarum laeveShrub14C labeling and defoliation experimentPhoto-synthateAcopetalThe daughter plants did not sacrifice their own growth when transporting the photosynthetic substance to the stressed mother plants.[24]
Acid fuchsin dye applicationWaterAcopetal/basipetalDepending upon the ramet level, the donor ramet delivered different water proportions to the recipient ramet.[23]
Mikania micranthaHerbConnecting/severing stemWater/photosynthate Relatively stable photosynthesis and specific leaf areas were maintained through clonal integration, but the resource allocation of ramets was changed.[10]
Buchloe dactyloidesHerbAcid fuchsin applicationWaterAcopetalThe chlorophyll fluorescence characteristics of the ortet were improved, increasing the ability of ramets to absorb nutrients.[31,97]
14C isotope labelingPhoto-synthateMainly acopetal
Glechoma longitubaHerbConnecting/severing stemPhoto-synthateMainly acopetalThe investment obtained by the stressed ramets was increased, and the leaf stomatal adaptation strategy improved survival rates and adaptation to the habitat.[98,99]
Zoysia japonica SteudHerb18O tracer techniqueWaterMainly acopetalThe distribution ratios of water transport were different in different structures of Zoysia japonica.[28]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Yang, P.; Huang, L.; He, S.; Zeng, X.; Chen, Y.; Wang, H. Adaptive Strategies Employed by Clonal Plants in Heterogeneous Patches. Forests 2023, 14, 1648. https://doi.org/10.3390/f14081648

AMA Style

Yang P, Huang L, He S, Zeng X, Chen Y, Wang H. Adaptive Strategies Employed by Clonal Plants in Heterogeneous Patches. Forests. 2023; 14(8):1648. https://doi.org/10.3390/f14081648

Chicago/Turabian Style

Yang, Pan, Li Huang, Suni He, Xianghua Zeng, Yinyi Chen, and Haimiao Wang. 2023. "Adaptive Strategies Employed by Clonal Plants in Heterogeneous Patches" Forests 14, no. 8: 1648. https://doi.org/10.3390/f14081648

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop