Cross-species multiple environmental stress responses: An integrated approach to identify candidate genes for multiple stress tolerance in sorghum (Sorghum bicolor (L.) Moench) and related model species

Abstract

BackgroundCrop response to the changing climate and unpredictable effects of global warming with adverse conditions such as drought stress has brought concerns about food security to the fore; crop yield loss is a major cause of concern in this regard. Identification of genes with multiple responses across environmental stresses is the genetic foundation that leads to crop adaptation to environmental perturbations.MethodsIn this paper, we introduce an integrated approach to assess candidate genes for multiple stress responses across-species. The approach combines ontology based semantic data integration with expression profiling, comparative genomics, phylogenomics, functional gene enrichment and gene enrichment network analysis to identify genes associated with plant stress phenotypes. Five different ontologies, viz., Gene Ontology (GO), Trait Ontology (TO), Plant Ontology (PO), Growth Ontology (GRO) and Environment Ontology (EO) were used to semantically integrate drought related information.ResultsTarget genes linked to Quantitative Trait Loci (QTLs) controlling yield and stress tolerance in sorghum (Sorghum bicolor (L.) Moench) and closely related species were identified. Based on the enriched GO terms of the biological processes, 1116 sorghum genes with potential responses to 5 different stresses, such as drought (18%), salt (32%), cold (20%), heat (8%) and oxidative stress (25%) were identified to be over-expressed. Out of 169 sorghum drought responsive QTLs associated genes that were identified based on expression datasets, 56% were shown to have multiple stress responses. On the other hand, out of 168 additional genes that have been evaluated for orthologous pairs, 90% were conserved across species for drought tolerance. Over 50% of identified maize and rice genes were responsive to drought and salt stresses and were co-located within multifunctional QTLs. Among the total identified multi-stress responsive genes, 272 targets were shown to be co-localized within QTLs associated with different traits that are responsive to multiple stresses. Ontology mapping was used to validate the identified genes, while reconstruction of the phylogenetic tree was instrumental to infer the evolutionary relationship of the sorghum orthologs. The results also show specific genes responsible for various interrelated components of drought response mechanism such as drought tolerance, drought avoidance and drought escape.ConclusionsWe submit that this approach is novel and to our knowledge, has not been used previously in any other research; it enables us to perform cross-species queries for genes that are likely to be associated with multiple stress tolerance, as a means to identify novel targets for engineering stress resistance in sorghum and possibly, in other crop species.

Pathways and Network Based Analysis of Candidate Genes to Reveal Cross-Talk and Specificity in the Sorghum (Sorghum bicolor (L.) Moench) Responses to Drought and It's Co-occurring Stresses

“…Such hub genes were reported previously in response to drought tolerance in various other crops (Hopper et al, 2016 ; Jaiswal et al, 2018 ). To this end, the significant association of enriched GO terms such as water deprivation; response to desiccation and salt; response to cold and heat and response to oxidative stresses with most of these genes in sorghum was shown to be empirical evidence for their involvement in regulatory and functional features of drought responses, concordant with the previous results in drought tolerance investigation in sorghum (Dugas et al, 2011 ; Woldesemayat et al, 2017 , 2018b ).…”

“…The molecular mechanism behind ABA signaling pathway involves ABA receptors (PYR/PYL/RCAR), protein phosphatases (PP2C), protein kinases (SnRK2), and the ABA-activated transcription factors and their downstream target genes to initiate stomatal closure (Lee and Luan, 2012 ) (Figure 3 ). A total of 37 ABA-inducible genes among others were found to be involved in ABA signal transduction including the 2 known universally expressed genes, Sb03g026070 and Sb09g030600, which were identified under responses to multiple environmental stresses such as cold, drought, heat, and salt stresses (Woldesemayat et al, 2018b ). Such widespread functionally diverse genes may be considered critical in sorghum drought tolerance, based on their inhibitory role in the plant hormone signal transduction (Leung and Giraudat, 1998 ), which is probably associated with their function to encode protein phosphatase 2C (PP2C; EC:3.1.3.16; K14497), an enzyme involved in the negative regulation of the ABA signaling pathway (Nishimura et al, 2010 ).…”

“…The candidate genes that were identified to be associated with responses to drought and other stresses such as heat, cold, salt, and oxidative stress were collected from the various data source that included association studies, gene expression profiles from sorghum, from literature search based on studies targeted on plant stress tolerance, and biological regulatory pathways. We identified and prioritized genes for drought tolerance in our previous studies (Woldesemayat et al, 2017 , 2018b ). We targeted these genes by selecting a list of 133 prioritized genes in the present study and combined with expression data for a comprehensive network and pathway cross-talk analysis using additional and updated data information (Table S1 ).…”

“…Whereas, the data contained in GSE80699 comprised 6 drought stressed samples and the other 6 control samples. In addition, we included candidate genes from stress datasets tested for salt, cold, heat, and oxidative stress tolerance (Woldesemayat et al, 2018b ) for comparison, because these stresses usually co-exist with drought stress compounding the effect on agricultural production and plant survival.…”

“…Previous studies elucidated that plant specific responses to stress combination may require over-expression of unique genesets which are different from the geneset over-expressed in plants exposed to individual stress (Rizhsky et al, 2002 ). Recently, drought stress response strategies were investigated in sorghum using integrated approaches, whereby genes for tolerance to multiple stresses were identified and evaluated across species (Woldesemayat et al, 2017 , 2018b ). Although, these investigations, hitherto, have increased our knowledge of stress tolerance mechanism mainly at physiobiochemical level, interaction between multiple individual stresses and stress combinations and the resulting cross-talk between signaling pathways should be studied so as to advance our understanding of molecular mechanism underling stress tolerance associated with natural conditions.…”