Research Article: Meta-analysis of drought-tolerant genotypes in Oryza sativa: A network-based approach

Date Published: May 6, 2019

Publisher: Public Library of Science

Author(s): Sanchari Sircar, Nita Parekh, Niranjan Baisakh.

http://doi.org/10.1371/journal.pone.0216068

Abstract

Drought is a severe environmental stress. It is estimated that about 50% of the world rice production is affected mainly by drought. Apart from conventional breeding strategies to develop drought-tolerant crops, innovative computational approaches may provide insights into the underlying molecular mechanisms of stress response and identify drought-responsive markers. Here we propose a network-based computational approach involving a meta-analytic study of seven drought-tolerant rice genotypes under drought stress.

Co-expression networks enable large-scale analysis of gene-pair associations and tightly coupled clusters that may represent coordinated biological processes. Considering differentially expressed genes in the co-expressed modules and supplementing external information such as resistance/tolerance QTLs, transcription factors, network-based topological measures, we identify and prioritize drought-adaptive co-expressed gene modules and potential candidate genes. Using the candidate genes that are well-represented across the datasets as ‘seed’ genes, two drought-specific protein-protein interaction networks (PPINs) are constructed with up- and down-regulated genes. Cluster analysis of the up-regulated PPIN revealed ABA signalling pathway as a central process in drought response with a probable crosstalk with energy metabolic processes. Tightly coupled gene clusters representing up-regulation of core cellular respiratory processes and enhanced degradation of branched chain amino acids and cell wall metabolism are identified. Cluster analysis of down-regulated PPIN provides a snapshot of major processes associated with photosynthesis, growth, development and protein synthesis, most of which are shut down during drought. Differential regulation of phytohormones, e.g., jasmonic acid, cell wall metabolism, signalling and posttranslational modifications associated with biotic stress are elucidated. Functional characterization of topologically important, drought-responsive uncharacterized genes that may play a role in important processes such as ABA signalling, calcium signalling, photosynthesis and cell wall metabolism is discussed. Further transgenic studies on these genes may help in elucidating their biological role under stress conditions.

Currently, a large number of resources for rice functional genomics exist which are mostly underutilized by the scientific community. In this study, a computational approach integrating information from various resources such as gene co-expression networks, protein-protein interactions and pathway-level information is proposed to provide a systems-level view of complex drought-responsive processes across the drought-tolerant genotypes.

Partial Text

Drought is an inevitable consequence of drastic climate change. A look at the World Drought Map for the year 2017 from the Global Drought Information System [1] reveals the severity and intensity of drought across the globe. At this juncture, meeting the nutritional demands for an ever-increasing population is a challenge for policy makers. Although drought and heat waves have destroyed nearly a tenth of the cereal harvests, populations across the world continue to depend on them for food.

The fascinating complexity of biological processes in plants is reflected in the intricate interactions in co-expression networks. With the availability of a large number of transcriptomic datasets in public repositories, co-expression network analysis allows us to integrate this information and perform large-scale multi-genic studies. On one hand, we need this complexity to infer functional annotations of genes from tightly connected neighborhood (‘guilt-by-association’), while on the other hand, we need to dissect the networks to remove noisy connections and identify critical biological processes. Various approaches have been proposed, e.g., construction of condition-dependent co-expression networks with context-specific interactions [174,175], split co-expression networks into functional modules which may represent tightly coordinated biological processes [176,177], use of functional and comparative genomics [178,179], etc.

In this study, a comprehensive analysis of the complex drought-responsive processes using an integrated, systems-level approach across seven drought tolerant rice genotypes is presented. Preliminary analysis of the co-expression network revealed that transcriptional regulatory processes, post-translational modifications followed by photosynthesis are at the forefront of drought response. With the integration of protein-protein interactions, a detailed view of the system is possible and critical processes which otherwise lay hidden are brought forth. The phytohormone abscisic acid is seen to play a central role in regulating the energy metabolism of cells. Protective mechanisms like the transcriptional activation of molecular chaperons, amino acid metabolism and cellular respiratory processes are enhanced. The down-regulation of photosynthetic machinery and cellulose-associated genes explains a cessation of aerial growth during drought stress. The antagonistic relationship observed between ABA and SA-dependent pathogen response pathways indicate increased susceptibility of plants to certain pathogens during drought.

 

Source:

http://doi.org/10.1371/journal.pone.0216068

 

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