The submergence tolerance regulator SUB1A differentially coordinates molecular adaptation to submergence in mature and growing leaves of rice (Oryza sativa L.).
Oryza sativa
hormones
leaf maturity
submergence
transcriptome
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
04 2022
04 2022
Historique:
revised:
06
12
2021
received:
13
09
2021
accepted:
20
12
2021
pubmed:
4
1
2022
medline:
6
4
2022
entrez:
3
1
2022
Statut:
ppublish
Résumé
A typical adaptive response to submergence regulated by SUB1A, the ethylene-responsive transcription factor gene, is the restricted elongation of the uppermost leaves. However, the molecular and physiological functions of SUB1A have been characterized using entire shoot tissues, most of which are mature leaves that do not elongate under submergence. We aimed to identify leaf-type-specific and overlapping adaptations coordinated in SUB1A-dependent and -independent manners. To this end, we compared the transcriptomic and hormonal responses to submergence between mature and growing leaves using rice genotypes with and without SUB1A. Monosaccharide, branched-chain amino acid, and nucleoside metabolism, associated with ATP synthesis, were commonly activated in both leaf types regardless of genotype. In both leaf types, pathways involved in carbohydrate and nitrogen metabolism were suppressed by SUB1A, with more severe restriction in growing leaves that have a greater energy demand if SUB1A is absent. In growing leaves, accumulation of and responsiveness to growth-regulating hormones were properly modulated by SUB1A, which correlated with restricted elongation. In mature leaves, submergence-induced auxin accumulation was suppressed by SUB1A. This study demonstrates that different sets of hormonal pathways, both of which are modulated by SUB1A, contribute to distinct adaptive responses to submergence in mature and growing rice leaves.
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
71-87Informations de copyright
© 2022 Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Alpuerto, J.B., Hussain, R.M.F. & Fukao, T. (2016) The key regulator of submergence tolerance, SUB1A, promotes photosynthetic and metabolic recovery from submergence damage in rice leaves. Plant, Cell and Environment, 39, 672-684.
Andrews S. (2010) FastQC: a quality control tool for high-throughput sequence data. Available from: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ [Accessed 27 August 2021].
Arnell, N.W. & Gosling, S.N. (2016) The impacts of climate change on river flood risk at the global scale. Climatic Change, 134, 387-401.
Baena-González, E. & Lunn, J.E. (2020) SnRK1 and trehalose 6-phosphate - two ancient pathways converge to regulate plant metabolism and growth. Current Opinion in Plant Biology, 55, 52-59.
Bailey-Serres, J., Fukao, T., Ronald, P., Ismail, A., Heuer, S. & Mackill, D. (2010) Submergence tolerant rice: SUB1’s journey from landrace to modern cultivar. Rice, 3, 138-147.
Bailey-Serres, J., Fukao, T., Gibbs, D.J., Holdsworth, M.J., Lee, S.C., Licausi, F. et al. (2012) Making sense of low oxygen sensing. Trends in Plant Science, 17, 129-138.
Barding, G.A., Fukao, T., Béni, S., Bailey-Serres, J. & Larive, C.K. (2012) Differential metabolic regulation governed by the rice SUB1A gene during submergence stress and identification of alanylglycine by 1H NMR spectroscopy. Journal of Proteome Research, 11, 320-330.
Barding, G.A., Béni, S., Fukao, T., Bailey-Serres, J. & Larive, C.K. (2013) Comparison of GC-MS and NMR for metabolite profiling of rice subjected to submergence stress. Journal of Proteome Research, 12, 898-909.
Benjamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B, 57, 289-300.
Birnbaum, K.D. & Sánchez, A.A. (2008) Slicing across kingdoms: regeneration in plants and animals. Cell, 132, 697-710.
Chakraborty, K., Guru, A., Jena, P., Ray, S., Guhey, A., Chattopadhyay, K. et al. (2021) Rice with SUB1 QTL possesses greater initial leaf gas film thickness leading to delayed perception of submergence stress. Annals of Botany, 127, 251-265.
Chauvaux, N., Van Dongen, W., Esmans, E.L. & Van Onckelen, H.A. (1997) Quantitative analysis of 1-aminocyclopropane-1-carboxylic acid by liquid chromatography coupled to electrospray tandem mass spectrometry. Journal of Chromatography A, 775, 143-150.
Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S. et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.
Donat, M.G., Lowry, A.L., Alexander, L.V., O'Gorman, P.A. & Maher, N. (2016) More extreme precipitation in the world's dry and wet regions. Nature Climate Change, 6, 508-513.
Du, M., Spalding, E.P. & Gray, W.M. (2020) Rapid auxin-mediated cell expansion. Annual Review of Plant Biology, 71, 379-402.
Fukao, T. & Bailey-Serres, J. (2008) Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice. Proceedings of the National Academy of Sciences of the United States of America, 105, 16814-16819.
Fukao, T. & Xiong, L. (2013) Genetic mechanisms conferring adaptation to submergence and drought in rice: simple or complex? Current Opinion in Plant Biology, 16, 196-204.
Fukao, T., Xu, K., Ronald, P.C. & Bailey-Serres, J. (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell, 18, 2021-2034.
Fukao, T., Yeung, E. & Bailey-Serres, J. (2011) The submergence tolerance regulator SUB1A mediates crosstalk between submergence and drought tolerance in rice. Plant Cell, 23, 412-427.
Fukao, T., Yeung, E. & Bailey-Serres, J. (2012) The submergence tolerance gene SUB1A delays leaf senescence under prolonged darkness through hormonal regulation in rice. Plant Physiology, 160, 1795-1807.
Fukao, T., Barrera-Figueroa, B.E., Juntawong, P. & Peña-Castro, J.M. (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied aspects. Frontiers in Plant Science, 10, 340.
Gallei, M., Luschnig, C. & Friml, J. (2020) Auxin signaling in growth: Schrödinger's cat out of the bag. Current Opinion in Plant Biology, 53, 43-49.
Garg, R., Tyagi, A.K. & Jain, M. (2012) Microarray analysis reveals overlapping and specific transcriptional responses to different plant hormones in rice. Plant Signaling and Behavior, 7, 951-956.
Gibbs, D.J., Lee, S.C., Md Isa, N., Gramuglia, S., Fukao, T., Bassel, G.W. et al. (2011) Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants. Nature, 479, 415-418.
Han, Y.Y., Chen, Y.H., Yin, S.H., Zhang, M. & Wang, W. (2015) Over-expression of TaEXPB23, a wheat expansin gene, improves oxidative stress tolerance in transgenic tobacco plants. Journal of Plant Physiology, 173, 62-71.
Hibara, K.I., Isono, M., Mimura, M., Sentoku, N., Kojima, M., Sakakibara, H. et al. (2016) Jasmonate regulates juvenile-to-adult phase transition in rice. Development, 143, 3407-3416.
Hildebrandt, T.M., Nunes Nesi, A., Araújo, W.L. & Braun, H.P. (2015) Amino acid catabolism in plants. Molecular Plant, 8, 1563-1579.
Hirabayashi, Y., Tanoue, M., Sasaki, O., Zhou, X. & Yamazaki, D. (2021) Global exposure to flooding from the new CMIP6 climate model projections. Scientific Reports, 11, 3740.
Jung, K.H., Seo, Y.S., Walia, H., Cao, P., Fukao, T., Canlas, P.E. et al. (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiology, 152, 1674-1692.
Li, A.X., Han, Y.Y., Wang, X., Chen, Y.H., Zhao, M.R., Zhou, S.M. et al. (2015) Root-specific expression of wheat expansin gene TaEXPB23 enhances root growth and water stress tolerance in tobacco. Environmental and Experimental Botany, 110, 73-84.
Liao, Y., Smyth, G.K. & Shi, W. (2014) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 30, 923-930.
Lin, C.C., Chao, Y.T., Chen, W.C., Ho, H.Y., Chou, M.Y., Li, Y.R. et al. (2019) Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. Proceedings of the National Academy of Sciences of the United States of America, 116, 3300-3309.
Locke, A.M., Barding, G.A., Sathnur, S., Larive, C.K. & Bailey-Serres, J. (2018) Rice SUB1A constrains remodelling of the transcriptome and metabolome during submergence to facilitate post-submergence recovery. Plant, Cell and Environment, 41, 721-736.
Love, M.I., Huber, W. & Anders, S. (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15, 550.
Lulsdorf, M.M., Yuan, H.Y., Slater, S.M.H., Vandenberg, A., Han, X., Zaharia, L.I. et al. (2013) Endogenous hormone profiles during early seed development of C. arietinum and C. anatolicum. Plant Growth Regulation, 71, 191-198.
Mustroph, A., Lee, S.C., Oosumi, T., Zanetti, M.E., Yang, H., Ma, K. et al. (2010) Cross-Kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiology, 152, 1484-1500.
Nghi, K.N., Tagliani, A., Mariotti, L., Weits, D.A., Perata, P. & Pucciariello, C. (2021) Auxin is required for the long coleoptile trait in japonica rice undersubmergence. New Phytologist, 229, 85-93.
Rankenberg, T., Geldhof, B., van Veen, H., Holsteens, K., Van de Poel, B. & Sasidharan, R. (2021) Age-dependent abiotic stress resilience in plants. Trends in Plant Science, 26, 692-705.
Riemann, M., Müller, A., Korte, A., Furuya, M., Weiler, E.W. & Nick, P. (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiology, 133, 1820-1830.
Sato, Y., Antonio, B.A., Namiki, N., Takehisa, H., Minami, H., Kamatsuki, K. et al. (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Research, 39, D1141-D1148.
Schmitz, A.J., Folsom, J.J., Jikamaru, Y., Ronald, P. & Walia, H. (2013) SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. New Phytologist, 198, 1060-1070.
Singh, P. & Sinha, A.K. (2016) A positive feedback loop governed by SUB1A1 interaction with mitogen-activated protein kinase3 imparts submergence tolerance in rice. Plant Cell, 28, 1127-1143.
Singh, S., Mackill, D.J. & Ismail, A.M. (2014) Physiological basis of tolerance to complete submergence in rice involves genetic factors in addition to the SUB1 gene. AoB Plants, 6, 1-20.
Skirycz, A. & Inzé, D. (2010) More from less: plant growth under limited water. Current Opinion in Biotechnology, 21, 197-203.
Skirycz, A., de Bodt, S., Obata, T., de Clercq, I., Claeys, H., de Rycke, R. et al. (2010) Developmental stage specificity and the role of mitochondrial metabolism in the response of Arabidopsis leaves to prolonged mild osmotic stress. Plant Physiology, 152, 226-244.
Skirycz, A., Claeys, H., de Bodt, S., Oikawa, A., Shinoda, S., Andriankaja, M. et al. (2011) Pause-and-stop: The effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell, 23, 1876-1888.
Tamang, B.G. & Fukao, T. (2015) Plant adaptation to multiple stresses during submergence and following desubmergence. International Journal of Molecular Sciences, 16, 30164-30180.
Tamang, B.G., Li, S., Rajasundaram, D., Lamichhane, S. & Fukao, T. (2021) Overlapping and stress-specific transcriptomic and hormonal responses to flooding and drought in soybean. Plant Journal, 107, 100-117.
Tian, T., Liu, Y., Yan, H., You, Q., Yi, X., Du, Z. et al. (2017) AgriGO v2.0: a GO analysis toolkit for the agricultural community, 2017 update. Nucleic Acids Research, 45, W122-W129.
Uji, Y., Taniguchi, S., Tamaoki, D., Shishido, H., Akimitsu, K. & Gomi, K. (2016) Overexpression of OsMYC2 results in the up-regulation of early JA-responsive genes and bacterial blight resistance in rice. Plant and Cell Physiology, 57, 1814-1827.
Valenzuela, C.E., Acevedo-Acevedo, O., Miranda, G.S., Vergara-Barros, P., Holuigue, L., Figueroa, C.R. et al. (2016) Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. Journal of Experimental Botany, 67, 4209-4220.
Vanneste, S. & Friml, J. (2009) Auxin: a trigger for change in plant development. Cell, 136, 1005-1016.
Winkel, A., Pedersen, O., Ella, E., Ismail, A.M. & Colmer, T.D. (2014) Gas film retention and underwater photosynthesis during field submergence of four contrasting rice genotypes. Journal of Experimental Botany, 65, 3225-3233.
Xu, K., Xu, X., Fukao, T., Canlas, P., Maghirang-Rodriguez, R., Heuer, S. et al. (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature, 442, 705-708.
Yang, D.L., Yao, J., Mei, C.S., Tong, X.H., Zeng, L.J., Li, Q. et al. (2012) Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proceedings of the National Academy of Sciences of the United States of America, 109, E1192-E1200.
Yu, S.M., Lo, S.F. & Ho, T.D. (2015) Source-sink communication: regulated by hormone, nutrient, and stress cross-signaling. Trends in Plant Science, 20, 844-857.
Zhao, Y., Chan, Z., Gao, J., Xing, L., Cao, M., Yu, C. et al. (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proceedings of the National Academy of Sciences of the United States of America, 113, 1949-1954.
Zheng, Y., Cui, X., Su, L., Fang, S., Chu, J., Gong, Q. et al. (2017) Jasmonate inhibits COP1 activity to suppress hypocotyl elongation and promote cotyledon opening in etiolated Arabidopsis seedlings. Plant Journal, 90, 1144-1155.