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ARS Home » Southeast Area » Raleigh, North Carolina » Soybean and Nitrogen Fixation Research » Research » Publications at this Location » Publication #343535
Title: Rice SUB1A constrains remodeling of the transcriptome and metabolome during submergence and post-submergence recovery”.

Author
item Locke, Anna
item BARDING , GREGORY - California Polytechnic State University
item SATHNUR, SUMUK - University Of California
item LARIVE, CYNTHIA - University Of California
item BAILEY-SERRES, JULIA - University Of California

Submitted to: Plant, Cell & Environment
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/11/2017
Publication Date: 4/1/2018
Citation: Locke, A.M., Barding, G.A., Sathnur, S., Larive, C.K., Bailey-Serres, J. 2018. Rice SUB1A constrains remodeling of the transcriptome and metabolome during submergence and post-submergence recovery”.. Plant, Cell & Environment. 41:721-736. https://doi.org/10.1111/pce.13094.
DOI: https://doi.org/10.1111/pce.13094

Interpretive Summary: The SUB1A gene confers flooding tolerance to rice plants by restricting growth during submergence, and the same gene may also improve other abiotic stress responses in rice. Although it has previously been shown that rice with SUB1A regains normal leaf water status and is able to resume photosynthesis more rapidly after submergence than submergence-intolerant varieties, the mechanisms behind this response as well as the extent of SUB1A’s transcriptional and metabolomic impact after flooding have not been investigated. This study used RNA-seq and a range of metabolomic techniques, including GC-MS, LC-MS, and NMR, to demonstrate that SUB1A continues to regulate transcription and carbon metabolism through a 24 hour submergence recovery period. Principal components analysis demonstrated that the transcriptome of submerged plants had nearly returned to the pre-submergence state after 24 hours of recovery. Recovery of the metabolome, however, lagged behind the transcriptome. Although photosynthesis, particularly PSII-related processes, have previously been found to be better maintained in Sub1 plants following flooding, this study showed that SUB1A does not directly improve photosynthetic capacity through transcription, although it had an impact on the transcript abundance of a gene known to influence chloroplast degradation. SUB1A plants particularly reduced the free amino acid accumulation that is characteristic for many abiotic stress responses, but this clear effect in the metabolome was not explained by major changes in transcription for amino acid metabolism. Overall the study highlighted the importance of SUB1A to plant recovery and physiological function well after flooding stress has ceased, and also demonstrated the importance of considering metabolism and physiological function in addition to transcription when evaluating the impact that a single gene may have on plant stress.

Technical Abstract: The rice (Oryza sativa L.) ethylene-responsive transcription factor SUB1A confers tolerance to prolonged, complete submergence by limiting underwater elongation growth. Rice encoding SUB1A-1 also recovers photosynthetic function and re-commences development towards flowering more rapidly after desubmergence, but the transcriptional and metabolic underpinnings of the transition from stress amelioration to developmental recommencement are not well known. Transcriptomic and metabolomic analyses were conducted to broadly identify mechanisms by which SUB1A improves physiological function over the 24 hours following a sub-lethal submergence event. Distinctions in the reconfiguration of the transcriptome and metabolome during submergence and re-aeration were uncovered between near-isogenic genotypes. Notable was the limited direct link to photosynthetic gene regulation, although SUB1A influenced the abundance of ca. 1400 transcripts and had a continued impact on metabolite content, particularly free amino acids, glucose, and sucrose, throughout the recovery period. SUB1A promoted rapid recovery of transcripts associated with growth but had limited influence on those associated with photosynthesis. The involvement of trehalose-6-phosphate (T6P) as a mediator of energy sensing during submergence was supported by depression of T6P content throughout submergence recovery, which was enhanced by SUB1A. This study extends prior demonstrations that SUB1A influences the transcriptome and metabolome during and following submergence, providing new evidence of converging signaling and metabolic pathways critical to rapidly reversible management of carbon and nitrogen metabolism.