Research articleDesi chickpea genotypes tolerate drought stress better than kabuli types by modulating germination metabolism, trehalose accumulation, and carbon assimilation
Introduction
Drought is a major constraint that restricts plant growth and development in chickpea. There are two major types of chickpea viz. desi and kabuli. Despite morphological differences between the desi and kabuli genotypes, they have a very narrow genetic base with up to 54% common genetic background (Upadhyaya et al., 2008; Varshney et al., 2013). However, the desi type can produce better yields under less than optimum conditions than the kabuli type (Nayyar et al., 2006; Yadav et al., 2006).
Drought decreases water and mineral uptake, photosynthesis and stomatal conductance (Farooq et al., 2009), all of which contribute to a substantial reduction in plant growth (Farooq et al., 2017a). Reduced water availability reduces plant growth due to a reduction in photosynthetic capacity and photosynthetic area (Chaves et al., 2011). Under limited water supply, the production of new leaves declines, and leaf abscission and senescence increases (Karamanos, 1980). As a result, total leaf area significantly decreases (Farooq et al., 2017a). Water deficit affects the photosynthetic apparatus due to the destruction of thylakoid membranes and disturbance of chlorophyll pigment formation (Tas and Tas, 2007). Drought may cause over-production of reactive oxygen species (ROS) (McCord, 2000), which causes oxidative damage to chloroplasts (Farooq et al., 2017a) through destabilization of the protein-pigment complex, and dilation of thylakoid membranes (Prasad and Saradhi, 2004). These ROS injure the DNA, nucleic acids, lipids, and proteins and may cause cell death (Foyer, 2005).
Plants respond to drought stress by closing stomata to restrict water loss (Liu et al., 2005; Awasthi et al., 2014), which reduces the influx of carbon (Awasthi et al., 2014) and, consequently, reduces photosynthesis due to decreased activities of ATP synthase and Rubisco (ribulose-1, 5-bisphosphate carboxylase) (Zlatev and Lidon, 2012).
The generation of ROS under water deficiency may act as a secondary messenger to activate defense mechanisms in plants (Farooq et al., 2009). Superoxide dismutase is the first line of defense to detoxify ROS to molecular oxygen and water to save the plant from oxidative damage (Noctor et al., 2000). The build-up of soluble phenolics and free proline also protects the plants from drought-induced oxidative damage (Farooq et al., 2009).
The accumulation of sugars, predominantly trehalose, protects plants from abiotic stresses (Farooq et al., 2017b) by restricting protein denaturation, acting as a free radical scavenger, and stabilizing biological membranes (Benaroudj et al., 2001). Trehalose also binds to the polar region of membranes with the hydroxyl group of proteins and phosphate to scavenge the ROS (Benaroudj et al., 2001; Farooq et al., 2009).
Plant responses to moisture deficit and tolerance are complex biological processes that need to be investigated using physiological and biochemical approaches at a systems level. Studies are available on chickpea tolerance to drought (Nayyar et al., 2006; Yadav et al., 2006), but there is limited information on the response of desi and kabuli chickpea genotypes to drought with special reference to transpiration efficiency (TE) and trehalose accumulation. This study hypothesized that the desi type of chickpea is more tolerant to drought due to morphological plasticity, and better TE and trehalose (and other sugars) accumulation. The specific objective of this study was to explore the basis of the differential response of desi and kabuli type chickpea genotypes to drought.
Section snippets
Planting material
Seeds of six desi (Bakhar-2011, Bitall-2016, BRC, Punjab-2008, NIAB-CH-2016, and Thal-2006) and six kabuli (CM-2008, K-9012, K-70005, Noor-2009, 2013 and Punajb-1) chickpea genotypes were collected from the Pulses Research Institute, Faisalabad, Pakistan.
Experiment 1
Chickpea seeds of the 12 tested genotypes were planted (eight seeds per pot) in soil-filled pots (10 kg). After emergence, the pots were thinned to six plants per pot and placed in a net-house under natural conditions. During the experiment,
Experiment 1
Drought significantly reduced seedling dry weight, SLA, and TE in both desi and kabuli chickpea types, relative to the well-watered controls (Table 1). Highest seedling dry weight was recorded in kabuli chickpea genotype K-70005 under well-watered conditions, which was followed kabuli chickpea genotype Noor-2013 and desi chickpea genotype Bakhar-2011 under well-watered. However, under drought stress, highest seedling dry weight was recorded in desi chickpea genotype Bitall-2016 followed by desi
Discussion
Drought stress affected the tested chickpea genotypes, with substantial genetic variation in the response of desi and kabuli chickpea types. Drought stress delayed emergence, which resulted in erratic and poor seedling growth and stand establishment in chickpea (Table 1, Table 2) due to reduced sugar metabolism, disturbed α-amylase activity (Table 3), decreased leaf CO2, PSII efficiency, and chlorophyll content (Table 4), oxidative damage (Table 5), reduced water relations (Table 6), and
Contribution
MF, SSA, and DJL conceived the idea, planned and conducted the experiment. MF and AU analyzed the data and prepared the first draft. MF, DJL, SSA, and KHMS wrote the final version of the manuscript.
Acknowledgments
The authors extend their appreciation to the International Scientific Partnership Program (ISPP) at King Saud University for funding this research work through ISPP# 0085.
References (55)
- et al.
Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals
J. Biol. Chem.
(2001) - et al.
Water deficit effects on root distribution of soybean, field pea and chickpea
Field Crop. Res.
(2006) Amylases α and β
- et al.
Recent advances in photosynthesis under drought and salinity
Adv. Bot. Res.
(2011) - et al.
Seed priming improves chilling tolerance in chickpea by modulating germination metabolism, trehalose accumulation and carbon assimilation
Plant Physiol. Biochem.
(2017) - et al.
Trehalose and plant stress responses: friend or foe?
Trends Plant Sci.
(2010) - et al.
Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation
Arch. Biochem. Biophys.
(1968) - et al.
A critical evaluation of traits for improving crop yields in water-limited environments
Adv. Agron.
(1990) - et al.
Cold, salinity and drought stresses: an overview
Arch. Biochem. Biophys.
(2005) The evolution of free radicals and oxidative stress
Am. J. Med.
(2000)
Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycine betaine biosynthesis into the chloroplasts
Plant Sci.
Variation in root traits of chickpea (Cicer arietinum L.) grown under terminal drought
Field Crop. Res.
Metabolite levels in specific cells and subcellular compartments of plant leaves
Methods Enzymol.
Osmotic adjustment, water relations and carbohydrate remobilization in pigeonpea under water deficits
J. Plant Physiol.
Copper enzymes in isolated chloroplast polyphenol oxidases in Beta vulgaris
Plant Physiol. (Wash. D C)
Chlorophyll stability is an indicator of drought tolerance in peanut
J. Agron. Crop Sci.
Seed Vigor Testing Handbook. Contribution No. 32 to the Handbook on Seed Testing
Individual and combined effects of transient drought and heat stress on carbon assimilation and seed filling in chickpea
Funct. Plant Biol.
A re-examination of the relative turgidity technique for estimating water deficit in leaves
Aust. J. Biol. Sci.
Rapid determination of free proline for water stress studies
Plant Soil
Seeds. Physiology of Development and Germination
Metabolic engineering for increased salt tolerance-the next step
Aust. J. Plant Physiol.
Determination of monosaccharides and disaccharides in honey by ion-exchange high performance chromatography
Acta Fac. Pharm. Univ. Comenianae
Indices of drought tolerance in wheat genotypes at early stages of plant growth
J. Agron. Crop Sci.
Colorimetric method for determination of sugars and related substances
Anal. Chem.
Plant drought stress: effects, mechanisms and management Agron
Sustain. Dev.
Drought stress in grain legumes during reproduction and grain filling
J. Agron. Crop Sci.
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