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Integrated multi-omics analysis reveals drought stress response mechanism in chickpea (Cicer arietinum L.)

ABSTRACT: Drought is one of the major constraints for crop productivity across the globe. Chickpea (Cicer arietinum L.) is mainly cultivated in the arid and semi-arid tropical regions under rain-fed conditions and drought stress is one of the major constraints, which causes up to 50% yield losses annually. In this study, transcriptomics, proteomics and metabolomics datasets from root tissues of contrasting drought responsive chickpea genotypes, ICC 4958 (drought-tolerant), JG 11 (drought-tolerant); an introgression line, JG 11+ (drought-tolerant) and ICC 1882, (drought-sensitive) under control and stress conditions were generated. The integrated analysis of these multi-omics data revealed complex molecular mechanism underlying drought stress response in chickpea. Transcriptomics integrated with proteomics data identified enhancement of hub proteins encoding isoflavone 4’-O-methyltransferase (Ca_06356), UDP-D-glucose/UDP-D-Galactose 4-epimerase (Ca_15037) and delta-1-pyrroline-5-carboxylate synthesis (Ca_24241). These proteins highlighted the involvement of critical pathways such as antibiotic biosynthesis, galactose metabolism and isoflavonoid biosynthesis in activating drought stress response mechanism. Subsequently, integration of metabolomics data identified six key metabolites (fructose, galactose, glucose, myo-inositol, galactinol and raffinose) that showed enhanced correlation with galactose metabolism. Further, integration of root -omics data together with genomic dataset of the “QTL-hotspot” region harbouring several drought tolerance related traits revealed involvement of candidate genes encoding aldo keto reductase family oxidoreductase (Ca_04551) and leucine rich repeat extensin 2 (Ca_04564). These results from integrated multi-omics approach provided a comprehensive understanding and new insights into the drought stress response mechanism of chickpea.

INSTRUMENT(S): LTQ Orbitrap Elite

ORGANISM(S): Cicer Arietinum (chickpea) (garbanzo)

TISSUE(S): Root

SUBMITTER: Palak Chaturvedi

LAB HEAD: Palak Chaturvedi

PROVIDER: PXD027033 | Pride | 2023-08-23

REPOSITORIES: Pride

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Dataset's files

Source:

			Action	DRS
	Chickpea_root_samples.xlsx	Xlsx
	Cicer_arietinum_GA_v1.0.gene.pep.fasta	Fasta
	ICC_1882_rep1_Control_root.raw	Raw
	ICC_1882_rep1_Stress_root.raw	Raw
	ICC_1882_rep2_Control_root.raw	Raw

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Project description:‘Pulsechip’, a boutique cDNA microarray, generated from a set of chickpea (Cicer arietinum L.) unigenes, grasspea (Lathyrus sativus L.) ESTs and lentil (Lens culinaris Med.) resistance gene analogs, was employed to generate an expression profile of chickpea accessions tolerant and susceptible to drought stress. Two groups of a tolerant and susceptible accession were challenged with drought stress. The experiments were performed in three biological replications. The experiments were conducted in reference design where respective tissues from unstressed plants served as control. The leaf and flower/bud tissues were collected and used for hybridization to measure changes in RNA abundance of treatment vs. control. The tissues from five experimental replicate plants per biological replication were pooled together (leaf and flower tissues separate) before RNA extraction. This RNA was used to prepare cDNA targets for expression analysis using microarray. The microarray had six technical replicate spots per EST. The transcript level for each EST/cDNA was firstly calculated as the average intensity of the six technical replicates and then the average intensity of three biological replicates. Data analysis included LOWESS normalization (LOcally WEighted polynomial regreSSion) to adjust for differences in quantity of initial RNA, labeling and detection efficiencies. A dye swap in one biological replicate adjusted dye bias, if any. The Differentially Expressed (DE) ESTs were identified as those with a 95% confidence interval for mean fold change (FC) that extended beyond the two-fold cut-off and also passed the Students t test (P<0.05) and FDR correction. These cut-offs translate into induced ESTs having a log2 ratio > 1 and repressed ESTs a ratio of < -1. The analysis consisted of three fold comparison. Firstly, the ESTs that were differentially expressed between treatment and control plants of each accession were detected. Then the ESTs that were similarly expressed by tolerant and susceptible accessions were then eliminated by comparison. This included a two-way comparison, where tolerant and susceptible genotypes were compared within and between groups. Lastly, ESTs that were consensually differentially expressed between tolerant and susceptible accessions of the two batches were identified. The hypothesis was that if a putative gene was consistently expressed only in tolerant or susceptible genotype for a particular stress, it might be a candidate for tolerance/susceptibility for that stress. Globally, the level of 114 transcripts was affected in response to drought stress in all the genotypes and tissue types studied. The DE transcripts in response to drought stress coded for various functional and regulatory proteins, most of which were repressed. Protein and other solute transport was repressed in susceptible-1 flowers but induced in tolerant-2 flowers, as evidenced by the induction of a protein-transport facilitation protein (DY475074) in flowers of tolerant-2 and repression of a aquaporin-like membrane channel protein (DY396334) and DNA-J like protein involved in intracellular protein transport (DY475488) in flowers of susceptible-1. Two putative auxin-repressed proteins (DY396289, DY396359) were highly repressed in flowers and leaves of tolerant-2, whilst being induced in flowers and leaves of susceptible-1. Defence-related genes including pathogenesis-related proteins (DY396305 and DY396343), nematode-resistance protein (CV793603), Cf-9 gene cluster (DY396352) and disease resistance response proteins (DY396265 and DY396276) were repressed in flowers of tolerant and susceptible genotypes. A Pea (pi230) disease resistance response protein (DY396390) and a multi-resistance protein ABC transporter (CV793605) were induced in flowers of both tolerant genotypes. Some genes involved in energy metabolism (DY396279 and DY475316) were repressed in leaves and flowers of tolerant and susceptible genotypes. Additionally, some transcripts related to senescence, including auxin responsive protein IAA9 (DY396315), senescence-associated protein DIN 1 (DY396338), and dehydration stress-induced protein (DY396321) were repressed in leaves and flowers of the tolerant genotypes. Of the 114 DE transcripts expressed in drought tolerant and susceptible genotypes, only two were consistently expressed. These included a cytosolic fructose 1,6-bisphosphatase (DY475548) and a gene with unknown function, which were repressed in flowers of both susceptible genotypes. Keywords: Chickpea, Drought stress, Tolerant, Susceptible, cDNA microarray

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Integrated multi-omics analysis reveals drought stress response mechanism in chickpea (Cicer arietinum L.)

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