Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat

Presently, pearl millet and wheat are belonging to highly important cereal crops. Pearl millet, however, is an under-utilized crop, despite its superior resilience to drought and heat stress in contrast to wheat. To investigate this in more detail, we performed comparative physiological screening an...

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Main Authors: Arindam Ghatak, Palak Chaturvedi, Gert Bachmann, Luis Valledor, Živa Ramšak, Mitra Mohammadi Bazargani, Prasad Bajaj, Sridharan Jegadeesan, Weimin Li, Xiaoliang Sun, Kristina Gruden, Rajeev K. Varshney, Wolfram Weckwerth
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2020.600278/full
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author Arindam Ghatak
Palak Chaturvedi
Gert Bachmann
Luis Valledor
Živa Ramšak
Mitra Mohammadi Bazargani
Prasad Bajaj
Sridharan Jegadeesan
Weimin Li
Xiaoliang Sun
Kristina Gruden
Rajeev K. Varshney
Wolfram Weckwerth
Wolfram Weckwerth
author_facet Arindam Ghatak
Palak Chaturvedi
Gert Bachmann
Luis Valledor
Živa Ramšak
Mitra Mohammadi Bazargani
Prasad Bajaj
Sridharan Jegadeesan
Weimin Li
Xiaoliang Sun
Kristina Gruden
Rajeev K. Varshney
Wolfram Weckwerth
Wolfram Weckwerth
author_sort Arindam Ghatak
collection DOAJ
description Presently, pearl millet and wheat are belonging to highly important cereal crops. Pearl millet, however, is an under-utilized crop, despite its superior resilience to drought and heat stress in contrast to wheat. To investigate this in more detail, we performed comparative physiological screening and large scale proteomics of drought stress responses in drought-tolerant and susceptible genotypes of pearl millet and wheat. These chosen genotypes are widely used in breeding and farming practices. The physiological responses demonstrated large differences in the regulation of root morphology and photosynthetic machinery, revealing a stay-green phenotype in pearl millet. Subsequent tissue-specific proteome analysis of leaves, roots and seeds led to the identification of 12,558 proteins in pearl millet and wheat under well-watered and stress conditions. To allow for this comparative proteome analysis and to provide a platform for future functional proteomics studies we performed a systematic phylogenetic analysis of all orthologues in pearl millet, wheat, foxtail millet, sorghum, barley, brachypodium, rice, maize, Arabidopsis, and soybean. In summary, we define (i) a stay-green proteome signature in the drought-tolerant pearl millet phenotype and (ii) differential senescence proteome signatures in contrasting wheat phenotypes not capable of coping with similar drought stress. These different responses have a significant effect on yield and grain filling processes reflected by the harvest index. Proteome signatures related to root morphology and seed yield demonstrated the unexpected intra- and interspecies-specific biochemical plasticity for stress adaptation for both pearl millet and wheat genotypes. These quantitative reference data provide tissue- and phenotype-specific marker proteins of stress defense mechanisms which are not predictable from the genome sequence itself and have potential value for marker-assisted breeding beyond genome assisted breeding.
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spelling doaj.art-0e5220e033a3410389e02556c3eb4dea2022-12-21T22:41:47ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-01-011110.3389/fpls.2020.600278600278Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to WheatArindam Ghatak0Palak Chaturvedi1Gert Bachmann2Luis Valledor3Živa Ramšak4Mitra Mohammadi Bazargani5Prasad Bajaj6Sridharan Jegadeesan7Weimin Li8Xiaoliang Sun9Kristina Gruden10Rajeev K. Varshney11Wolfram Weckwerth12Wolfram Weckwerth13Molecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaMolecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaMolecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaPlant Physiology Lab, Organisms and Systems Biology, Faculty of Biology, University of Oviedo, Oviedo, SpainDepartment of Systems Biology and Biotechnology, National Institute of Biology, Ljubljana, SloveniaAgriculture Institute, Iranian Research Organization for Science and Technology, Tehran, IranCenter of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, IndiaPremas Life Sciences, Bengaluru, IndiaMolecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaVienna Metabolomics Center (VIME), University of Vienna, Vienna, AustriaDepartment of Systems Biology and Biotechnology, National Institute of Biology, Ljubljana, SloveniaCenter of Excellence in Genomics & Systems Biology, International Crops Research Institute for the Semi-Arid Tropics, Hyderabad, IndiaMolecular Systems Biology Lab (MOSYS), Department of Functional and Evolutionary Ecology, University of Vienna, Vienna, AustriaVienna Metabolomics Center (VIME), University of Vienna, Vienna, AustriaPresently, pearl millet and wheat are belonging to highly important cereal crops. Pearl millet, however, is an under-utilized crop, despite its superior resilience to drought and heat stress in contrast to wheat. To investigate this in more detail, we performed comparative physiological screening and large scale proteomics of drought stress responses in drought-tolerant and susceptible genotypes of pearl millet and wheat. These chosen genotypes are widely used in breeding and farming practices. The physiological responses demonstrated large differences in the regulation of root morphology and photosynthetic machinery, revealing a stay-green phenotype in pearl millet. Subsequent tissue-specific proteome analysis of leaves, roots and seeds led to the identification of 12,558 proteins in pearl millet and wheat under well-watered and stress conditions. To allow for this comparative proteome analysis and to provide a platform for future functional proteomics studies we performed a systematic phylogenetic analysis of all orthologues in pearl millet, wheat, foxtail millet, sorghum, barley, brachypodium, rice, maize, Arabidopsis, and soybean. In summary, we define (i) a stay-green proteome signature in the drought-tolerant pearl millet phenotype and (ii) differential senescence proteome signatures in contrasting wheat phenotypes not capable of coping with similar drought stress. These different responses have a significant effect on yield and grain filling processes reflected by the harvest index. Proteome signatures related to root morphology and seed yield demonstrated the unexpected intra- and interspecies-specific biochemical plasticity for stress adaptation for both pearl millet and wheat genotypes. These quantitative reference data provide tissue- and phenotype-specific marker proteins of stress defense mechanisms which are not predictable from the genome sequence itself and have potential value for marker-assisted breeding beyond genome assisted breeding.https://www.frontiersin.org/articles/10.3389/fpls.2020.600278/fullclimate resiliencesenescencecerealsdrought stressproteomicsstay-green trait
spellingShingle Arindam Ghatak
Palak Chaturvedi
Gert Bachmann
Luis Valledor
Živa Ramšak
Mitra Mohammadi Bazargani
Prasad Bajaj
Sridharan Jegadeesan
Weimin Li
Xiaoliang Sun
Kristina Gruden
Rajeev K. Varshney
Wolfram Weckwerth
Wolfram Weckwerth
Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
Frontiers in Plant Science
climate resilience
senescence
cereals
drought stress
proteomics
stay-green trait
title Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
title_full Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
title_fullStr Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
title_full_unstemmed Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
title_short Physiological and Proteomic Signatures Reveal Mechanisms of Superior Drought Resilience in Pearl Millet Compared to Wheat
title_sort physiological and proteomic signatures reveal mechanisms of superior drought resilience in pearl millet compared to wheat
topic climate resilience
senescence
cereals
drought stress
proteomics
stay-green trait
url https://www.frontiersin.org/articles/10.3389/fpls.2020.600278/full
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