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International Journal of Molecular Sciences
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24 September 2021

Exploitation of Drought Tolerance-Related Genes for Crop Improvement

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1
National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, China
2
International Maize and Wheat Improvement Center, Texcoco 56237, Mexico
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Int. J. Mol. Sci.2021, 22(19), 10265;https://doi.org/10.3390/ijms221910265
This article belongs to the Special Issue Novel Approaches to Improve Abiotic Stress Tolerance in Crop Plants
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Abstract

Drought has become a major threat to food security, because it affects crop growth and development. Drought tolerance is an important quantitative trait, which is regulated by hundreds of genes in crop plants. In recent decades, scientists have made considerable progress to uncover the genetic and molecular mechanisms of drought tolerance, especially in model plants. This review summarizes the evaluation criteria for drought tolerance, methods for gene mining, characterization of genes related to drought tolerance, and explores the approaches to enhance crop drought tolerance. Collectively, this review illustrates the application prospect of these genes in improving the drought tolerance breeding of crop plants.

1. Introduction

With population growth and climate change, food security has become a major global challenge. It is predicted that the rising demand will require a two-fold increase of food production by 2050 [1]. Crop production is being impacted by increasing abiotic stresses. Drought is one of the most severe abiotic stresses on crop production, and its impact depends on its timing, duration, and intensity, caused by insufficient rainfall and/or altered precipitation patterns. According to the Intergovernmental Panel on Climate Change reports, the annual area of dry lands during 1961–2013 has increased at a rate of average of more than 1% per year. In 2015, around 500 million people experienced desertification [2]. Future droughts are predicted to be more frequent, severe, and longer-lasting [3]. Therefore, it is urgent to accelerate the genetic improvement of crop drought tolerance by using desirable genes through the application of new biotechnological tools.
In the history of crop breeding, conventional techniques such as cross, backcross, artificial mutagenesis, pedigree selection, and recurrent selection have played an important role in the genetic improvement of drought tolerance. Conventional breeding mainly relies on phenotypic selection in the field; however, it is greatly affected by the environmental conditions and requires many years of identification and evaluation, resulting in highly labor-intensive, time-consuming, and low efficiency. To accelerate drought tolerance breeding, it is vital to understand the physiological and genetic basis of crop responses to drought. However, drought tolerance is a complex quantitative trait controlled by multiple genetic loci and susceptible to environmental influences. Therefore, in the present review, the evaluation criteria of crop drought tolerance were reviewed, followed by mining approaches of drought tolerance genes and methods to improve the drought tolerance of crops.

2. Crop Drought Tolerance Evaluation Criteria

The drought tolerance evaluation criteria are dependent on the timing, duration, and intensity of drought stress, climatic conditions, measurement time, location, and instruments. It is the first step of crop drought tolerance breeding to select appropriate criteria to evaluate the drought tolerance of crops in a specific period and within a specific environment. The following selection criteria have been used to distinguish drought tolerance genotypes.

2.1. Agronomic Criteria

2.1.1. Morphological Traits

The visible phenotypes of plants can be used as an indicator of crop drought tolerance. For example, the rate and speed of seed germination, length of coleoptile, speed of leaf emergence, plant height, panicle neck diameter, wax content, survival rate under extreme drought, days to heading, seed setting rate, normalized difference vegetation index (NDVI), plant biomass, and their variations under different water regimes have been associated with drought tolerance [4].
Besides the above morphological traits, leaf morphology, including leaf length, width, thickness and color, leaf distribution, and stomatal characteristics, is highly responsive to a water deficit. Leaf rolling is also a typical physiological phenomenon under drought stress. Crop plants with moderately rolled leaves are thought to reduce water loss by transpiration [5]. Drought-tolerant plants tend to have some common phenotypes, such as smaller and thicker leaves, smaller and denser stomata, more epidermal trichomes, thicker cuticle epidermis and palisade tissue, and well-developed vascular bundle sheath.
Root architecture traits, such as the root number, diameter, angle, depth, total length, distribution, and biomass, are also highly associated with drought tolerance. Despite the importance of root traits in crop drought tolerance, they are rarely used directly as the selection criteria in breeding, because the phenotypic detection of root-related traits is a time-consuming and laborious process. Nonetheless, the root depth shows a strong association with a cooler canopy temperature, which can be used as a proxy in selection [6].

2.1.2. Yield-Related Traits

Yield-related traits such as the yield index (YI), yield stability index (YSI), harvest index (HI), water use (WU), and yield based water use efficiency (WUE) were used to evaluate the performances of genotypes under drought stress and limited irrigation conditions [7].

2.2. Physiological and Biochemical Criteria

Plants have evolved a series of mechanisms to withstand drought stress not only at the morphological level but, also, at the physiological and biochemical levels. The physiological and biochemical characteristics of plants in response to water stress include the capacities of photosynthesis, osmotic adjustment, antioxidant defense, the hormone level, and enzyme activity [8].

2.2.1. Photosynthesis-Related Traits

Drought severely decreases CO2 assimilation and affects photosynthesis by reducing the stomatal aperture and the concentration and activities of photosynthetic enzymes. Chlorophyll fluorescence is a relatively high throughput parameter to indicate photoinhibition due to a water deficit [9]. Fluorescence parameters were used to detect the changes of CO2 assimilation, linear electron flux, and photosystem II photochemistry under drought stress. Fluorescence imaging can be used to screen a large number of plants with photosynthetic perturbation under drought conditions. Crops with higher chlorophyll contents have a more efficient utilization of light energy and stronger drought tolerance under drought stress [10].

2.2.2. Osmotic Adjustment-Related Traits

Since plants accumulate a variety of substances to maintain cell growth and leaf turgor, the concentration of these substances can reflect the crop drought tolerance to a certain extent. These substances can be classified into two catalogs: (1) inorganic ions, such as K+ and Cl−; (2) organic substances, such as trehalose, fructan, mannitol, proline, glycine, and betaine; and low molecular weight proteins such as late embryogenesis abundant (LEA) proteins, aquaporins (AQP), osmotin, and molecular chaperones.

2.2.3. Antioxidant Defense-Related Traits

Oxidative stress is commonly accompanied by drought stress. Reactive oxygen species (ROS) stress may disturb the membrane protein and enzyme configuration [11]. The protective enzymes, such as superoxide dismutase (SOD), catalase (CAT), and peroxiredoxin (POD), are involved in reducing the ROS. Therefore, crop drought tolerance largely depends on the concentration of ROS and the activities of these protective enzymes.

2.2.4. Phytohormones-Related Traits

Among the endogenous phytohormones, abscisic acid (ABA) is regarded as the most closely related plant hormone to drought stress response. Drought stress induces the biosynthesis and accumulation of intracellular ABA, mainly in the root cap and wilted leaves, which activates the corresponding transcription factors and then promotes the expression of downstream drought-related genes [12].

2.3. Integrated Drought Tolerance Criteria

Predicting crop drought tolerance based on the expression of morphological traits and/or physiological and biochemical characters is an essential step in breeding drought-tolerant crops. However, it is not easy to accurately evaluate the crop drought tolerance due to its complexity. Research has focused on investigating the efficiency of several criteria and integrating these criteria in identifying crop genotypes, combining the drought tolerance and high yield potential under stressed and nonstressed environments. Sahar et al. compared 24 indices and found strong positive correlations between the grain yield and nine indices, such as the mean productivity (MP), geometric mean productivity (GMP), stress tolerance index (STI), mean relative performance (MRP), relative efficiency index (REI), modified stress tolerance indices 1 and 2 (MSTIk), harmonic mean of yield (HM), and relative decrease in yield (RDY), which can be used for selecting drought tolerant and high-yield genotypes [13]. Khalili et al. proposed an integrated selection criterion index (SI) similar to MP, GMP, STI, stress susceptibility (SSI), and YSI as an effective selection criterion to distinguish the tolerant and desirable genotypes across multiple environments [14].

2.4. High-Throughput Phenotyping Platform

The emergence of a high-throughput phenotyping (HTP) platform makes it possible to capture trait information from a large number of plant samples under different water regimes [15]. The HTP platform integrated multiple imaging techniques, including red–green–blue (RGB), thermal infrared (TIR), chlorophyll fluorescence (ChlF), and multispectral and hyperspectral imaging and other sensor equipment [16]. Besides ground-based imaging, aerial imaging by unmanned aerial vehicles is also used to monitor the responses of crops to drought [17]. HTP technology provides a strong support for dissecting the genetic basis of drought tolerance in crops.

5. Genetic Improvement of Drought Tolerance in Crops

In the history of crop breeding, breeders have unconsciously selected target genes by evaluating phenotypic traits. However, conventional breeding, which relies on multilocation phenotypic selection for many years, is inefficient. The application of molecular breeding technology will facilitate the direct selection of genotypes, speed up the breeding process, and improve the efficiency of developing drought-tolerant varieties.

5.1. Marker-Assisted Selection

Marker-assisted selection (MAS) is a selection strategy based on QTL or gene markers employed by breeders to accelerate plant breeding programs. According to the purpose of selection, MAS can be divided into marker-assisted pedigree selection (MAPS), genomic selection (GS) or genome-wide selection (GWS), marker-assisted recurrent selection (MARS), and marker-assisted backcrossing (MABC). Gupta et al. [132] reviewed the wheat genetics of important quantitative traits, including a tolerance to abiotic stress, and summarized the potential value of QTLs for the improvement of drought tolerance using MAS. Despite the availability of a large number of major QTL for drought tolerance, little progress has been made for MAS. For example, in rice, the pyramiding of six large-effect QTL for drought adaptation has improved the drought tolerance of Asian cultivars [133]. In wheat, using MAS, a major QTL (Qyld.csdh.7AL) was introgressed into wheat cultivars to develop a high-yield genotype under rainfed conditions [134]; the introgression of QTL on 7AS and 2BS led to the improvement of the grain yield under the drought treatment [135]. Functional molecular markers of candidate genes for drought tolerance have also been developed for use in breeding [136].

5.2. Genomic Selection

MAS has been implemented for crop breeding, but its efficiency is limited due to the small number of molecular markers that can be used. Drought and most agronomic traits are quantitative traits controlled by multiple minor effect genes. Using genome-wide markers to predict the breeding values of individuals, genomic selection as a promising breeding method presents a new alternative to traditional MAS [137]. GS has been shown to improve the efficiency and speed up breeding in maize [138], rice [139], and wheat [140], and high prediction accuracies have been obtained for the yield and a number of other traits. However, due to the genetic complexity of its characteristics, the genomic selection for improving drought tolerance should be investigated.

5.3. Genetic Improvement Using Transgene and Genome Editing Techniques

Along with the identification of the candidate genes, we can also use transgenic technology to improve the crop drought tolerance, such as OE, RNAi, VIGS, ZFN, TALEN, and CRISPR [141]. At present, genetically modified crops are widely used in the world. The genes used in transgenic crops mainly include herbicide resistance gene (Bar), insect resistance gene (Bt), and disease resistance genes, while drought tolerance genes are rarely used. Transgenic technology and gene editing technology will promote the genetic improvement of crop drought resistance. For example, CRISPR technologies can not only introduce a small insertion or deletion mutations at the target loci but can also provide precision editing, such as base editing, prime editing, and gene targeting [142].

5.4. Genetic Improvement Combined with the Chemical Approach

As an important hormone, ABA plays a vital role in the drought tolerance of crops, while, due to the chemical instability, the rapid catabolism of ABA limits its application in the field. Scientists have conducted vast amounts of research to search for more stable ABA analogs, such as pyrabactin, AM1 (ABA mimic 1)/quinabactin, cyanabactin, opabactin, and AMFs [143]. Furthermore, combining chemical and genetic approaches, AMFs are applied to PYL2 overexpression transgenic plants, increasing their drought tolerance [144]. Another avenue to improve crop drought tolerance is engineering an ABA receptor. An ABA receptor PYR1 variant, which is sensitive to the agrochemical mandipropamid, improved the drought tolerance in transgenic plants [145].

5.5. Molecular Design Breeding

Molecular design breeding, a highly integrated system based on biotechnology and bioinformatics [146], may be an effective approach to enhance drought tolerance [147]. It can design and manipulate genotypes to meet various breeding objectives in different ecological regions under diverse water conditions [148]. Based on the principle of molecular design breeding, the ideal genotypes can be identified during crossing, selection and transgene and genome editing.

6. Conclusions and Perspectives

Most transgenic plants with drought tolerance phenotypes were based on the overexpression of genes using constitutive promoters, such as actin, CaMV35S, and ubiquitin. However, the overexpression of genes is often accompanied by a yield penalty due to stress-induced energy consumption. Therefore, mining drought tolerance-related genes that are not subjected to yield penalties or fine-tuning these genes through suitable stress-inducible promoters to minimize the yield penalties should be considered [149].
Most of the genes reviewed in this paper have been shown to enhance drought tolerance in growth chambers or greenhouses, and the utility of most of the genes has not been verified in the field. This is especially problematic for water stress, since root growth in pots in controlled environments cannot be compared to their response in deep soil water profiles, which has a profound impact on their adaptation and productivity. Therefore, the use of these drought-tolerant genes in crop breeding still needs the joint efforts of scientists and breeders to achieve a proof of concept.
Crop plants are subjected to drought stress at various stages of growth and development. Plants can adapt to drought stress through a series of morphological, physiological, and biochemical changes, but these genetically regulated responses are extremely complex. Therefore, it is necessary to conduct phenotypic and genotypic identification and evaluation through multidisciplinary approaches and to comprehensively use conventional, physiological, and molecular breeding techniques to improve the drought tolerance of crops (Figure 1).
Figure 1. Approaches of breeding for drought tolerance in crops.

Author Contributions

R.J., X.M. and J.W. designed the outline; J.W. and C.L. wrote the manuscript; R.J. and L.L. revised the manuscript; and M.R. revised the manuscript and gave constructive comments. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Key R&D Program of China (2017YFD0300202) and the Agricultural Science and Technology Innovation Program (CAAS-ZDRW202002).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

AAOABA-aldehyde oxidase
ABAAbscisic acid
AQPAquaporins
AREB/ABFABA-responsive element-binding proteins/factors
CDPKCalcium dependent protein kinase
CGASCandidate gene association study
CIPKCalcineurin B-like interacting protein kinase
CSPCold shock protein
DREB/CBFDehydration responsive element binding protein/C-repeat binding factor
GWASGenome wide association studies
HTPHigh throughput phenotyping
LEALate embryogenesis abundant
MAPKMitogen-activated protein kinase
MASMarker-assisted selection
PYR1/PYL/RCARPyrabactin resistance 1/PYR1-like/Regulatory components of the ABA receptor
QTLQuantitative trait loci
RLKReceptor like kinase
ROSReactive oxygen species
SnRK2Sucrose nonfermenting related kinase 2
SODSuperoxide dismutase
TPSTrehalose-6-phosphate synthase

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Genome-Wide Identification and Characterization of the Cystatin Gene Family in Bread Wheat (Triticum aestivum L.)
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