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Rice Transcriptomics Reveal the Genetic Determinants of An In Planta Photorespiratory Bypass: a Novel Way to Increase Biomass in C3 Plants

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Abstract

Developing C4 rice is one of the global research challenges for yield improvement. In the optimal environment, the key difference between C3 and C4 plants with reference to biomass accumulation is photorespiration. Photorespiration is important for a plant’s survival. In spite of the high energy cost and carbon loss, diversion of a significant part of carbon from photorespiration to enrich CO2 concentration (preventing carbon loss) was opted for. Installation of photorespiratory bypasses was reported to improve biomass and yield in C3 plants. The contribution of non-foliar photosynthesis to yield improvement was well documented. However, its underlying genetic differences, when compared to foliar photosynthesis, are a research gap. In three rice genotypes (APO, BAM4234, and CROSSA), we compared the expression levels (for genes associated with photosynthesis and photorespiration) between the photosynthetic non-foliar (3–5-day old developing grains and peduncle) and foliar (flag leaf) organs to understand their differential expression pattern using an RNA-seq approach. Significant downregulation of the genes of photorespiration was observed in non-foliar photosynthetic tissue (3–5 dpa old developing grains) when compared to the flag leaves. Simultaneously, our study also revealed significant upregulation of the chloroplastic pyruvate dehydrogenase (cpPDC, BGIOSGA015796) gene in developing grains, when compared to the flag leaf, in all three genotypes. The occurrence of an in planta photorespiratory bypass in the photosynthetic tissues of the developing grains in rice is proposed. Enhanced expression levels for the cpPdc gene in the foliar tissues will potentially install a photorespiratory bypass for enhanced biomass accumulation and thereby yield.

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Data Availability

The data and sequence information were provided in the supplementary information of the manuscript. Additionally, the transcriptome raw reads for 18 samples (three genotypes, three tissues, and two replicates) were submitted in public database and is available at E-MTAB-8361. https://www.ebi.ac.uk/arrayexpress/experiments/E-MTAB-8361/

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Acknowledgements

The authors acknowledge M/s NxGenBio Life Sciences, Delhi, for the outsourced sequencing services and Mr. Nitesh Bandhiwal of this firm for his technical help. The authors also acknowledge the access for the supercomputing facility “ASHOKA.” We are grateful to Govindjee Govindjee (of the University of Illinois at Urbana-Champaign, USA) and Robert Henry (of the University of Queensland at St Lucia, Australia), for their critical inputs, comments, and suggestions. The authors also thank the anonymous reviewers for their inputs and comments.

Funding

Funding was supported by the Indian Council of Agricultural Research, through the research scheme “Incentivizing research in agriculture” program.

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Authors and Affiliations

  1. Division of Genomic Resources, ICAR-National Bureau of Plant Genetic Resources, PUSA Campus, New Delhi, 110012, India

    Parimalan Rangan, Dhammaprakash P. Wankhede, Rajkumar Subramani, Pooja Pathania, Arti Bartwal & Kuldeep Singh

  2. Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, St. Lucia, QLD, 4072, Australia

    Parimalan Rangan

  3. Division of Plant Physiology, ICAR-Indian Agricultural Research Institute, PUSA Campus, New Delhi, 110012, India

    Viswanathan Chinnusamy

  4. Tissue Culture and Cryo-Preservation Unit, ICAR-National Bureau of Plant Genetic Resources, PUSA Campus, New Delhi, 110012, India

    Surendra K. Malik

  5. Crop Physiology and Biochemistry Division, ICAR-National Rice Research Institute, Cuttack, 753006, India

    Mirza Jaynul Baig

  6. Centre for Agricultural Bioinformatics, ICAR-Indian Agricultural Statistics Research Institute, PUSA Campus, New Delhi, 110012, India

    Anil Rai

  7. Present Address: Genetic Resources Division, ICRISAT, Patancheru, Hyderabad, India

    Kuldeep Singh

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  1. Parimalan Rangan
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Contributions

Conceptualization, PR; Formal investigation, analysis and supervision, PR, DW, RS; Funding acquisition, SM, MJB; Methodology, PR, DW, RS, VC, PP, AB; Resources, VC, MJB, AR,KS; Writing – original draft, PR; Writing—review and editing, PR, VC, KS, RS, DW,MJB.

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Rangan, P., Wankhede, D.P., Subramani, R. et al. Rice Transcriptomics Reveal the Genetic Determinants of An In Planta Photorespiratory Bypass: a Novel Way to Increase Biomass in C3 Plants. Plant Mol Biol Rep (2024). https://doi.org/10.1007/s11105-024-01469-y

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