TY - JOUR
T1 - Natural variation in the chickpea metabolome under drought stress
AU - Chaturvedi, Palak
AU - Pierides, Iro
AU - López-Hidalgo, Cristina
AU - Garg, Vanika
AU - Zhang, Shuang
AU - Barmukh, Rutwik
AU - Bellaire, Anke
AU - Li, Jiahang
AU - Bachmann, Gert
AU - Valledor, Luis
AU - Varshney, Rajeev K
AU - Ghatak, Arindam
AU - Weckwerth, Wolfram
N1 - Publisher Copyright:
© 2024 The Author(s). Plant Biotechnology Journal published by Society for Experimental Biology and The Association of Applied Biologists and John Wiley & Sons Ltd.
PY - 2024/12
Y1 - 2024/12
N2 - Chickpea is the world's fourth largest grown legume crop, which significantly contributes to food security by providing calories and dietary protein globally. However, the increased frequency of drought stress has significantly reduced chickpea production in recent years. Here, we have performed a field experiment with 36 diverse chickpea genotypes to evaluate grain yield, photosynthetic activities and molecular traits related to drought stress. For metabolomics analysis, leaf tissue was collected at three time points representing different pod-filling stages. We identified L-threonic acid, fructose and sugar alcohols involved in chickpea adaptive drought response within the mid-pod-filling stage. A stress susceptibility index for each genotype was calculated to identify tolerance capacity under drought, distributing the 36 genotypes into four categories from best to worst performance. To understand how biochemical mechanisms control different traits for genetic improvement, we performed a differential Jacobian analysis, which unveiled the interplay between various metabolic pathways across three time points, including higher flux towards inositol interconversions, glycolysis for high-performing genotypes, fumarate to malate conversion, and carbon and nitrogen metabolism perturbations. Metabolic GWAS (mGWAS) analysis uncovered gene candidates involved in glycolysis and MEP pathway corroborating with the differential biochemical Jacobian results. Accordingly, this proposed data analysis strategy bridges the gap from pure statistical association to causal biochemical relations by exploiting natural variation. Our study offers new perspectives on the genetic and metabolic understanding of drought tolerance-associated diversity in the chickpea metabolome and led to the identification of metabolic control points that can be also tested in other legume crops.
AB - Chickpea is the world's fourth largest grown legume crop, which significantly contributes to food security by providing calories and dietary protein globally. However, the increased frequency of drought stress has significantly reduced chickpea production in recent years. Here, we have performed a field experiment with 36 diverse chickpea genotypes to evaluate grain yield, photosynthetic activities and molecular traits related to drought stress. For metabolomics analysis, leaf tissue was collected at three time points representing different pod-filling stages. We identified L-threonic acid, fructose and sugar alcohols involved in chickpea adaptive drought response within the mid-pod-filling stage. A stress susceptibility index for each genotype was calculated to identify tolerance capacity under drought, distributing the 36 genotypes into four categories from best to worst performance. To understand how biochemical mechanisms control different traits for genetic improvement, we performed a differential Jacobian analysis, which unveiled the interplay between various metabolic pathways across three time points, including higher flux towards inositol interconversions, glycolysis for high-performing genotypes, fumarate to malate conversion, and carbon and nitrogen metabolism perturbations. Metabolic GWAS (mGWAS) analysis uncovered gene candidates involved in glycolysis and MEP pathway corroborating with the differential biochemical Jacobian results. Accordingly, this proposed data analysis strategy bridges the gap from pure statistical association to causal biochemical relations by exploiting natural variation. Our study offers new perspectives on the genetic and metabolic understanding of drought tolerance-associated diversity in the chickpea metabolome and led to the identification of metabolic control points that can be also tested in other legume crops.
KW - Cicer/genetics
KW - Metabolome/genetics
KW - Droughts
KW - Genotype
KW - Stress, Physiological/genetics
KW - Plant Leaves/metabolism
KW - Genome-Wide Association Study
KW - Lyapunov equation
KW - stress susceptibility index (SSI)
KW - Cicer arietinum
KW - metabolomics
KW - metabolic GWAS
KW - data-driven control analysis
UR - http://www.scopus.com/inward/record.url?scp=85206673208&partnerID=8YFLogxK
U2 - 10.1111/pbi.14447
DO - 10.1111/pbi.14447
M3 - Article
C2 - 39411896
SN - 1467-7644
VL - 22
SP - 3278
EP - 3294
JO - Plant Biotechnology Journal
JF - Plant Biotechnology Journal
IS - 12
ER -