Multi-stress Resilience in Plants Recovering from Submergence

Overview

Journal Plant Biotechnol J

Specialties Biology
Biotechnology

Date 2022 Oct 11

PMID 36217562

Authors

Li-Bing Yuan

Mo-Xian Chen

Lin-Na Wang

Rashmi Sasidharan

Laurentius A C J Voesenek

Shi Xiao

Affiliations

Soon will be listed here.

Abstract

Submergence limits plants' access to oxygen and light, causing massive changes in metabolism; after submergence, plants experience additional stresses, including reoxygenation, dehydration, photoinhibition and accelerated senescence. Plant responses to waterlogging and partial or complete submergence have been well studied, but our understanding of plant responses during post-submergence recovery remains limited. During post-submergence recovery, whether a plant can repair the damage caused by submergence and reoxygenation and re-activate key processes to continue to grow, determines whether the plant survives. Here, we summarize the challenges plants face when recovering from submergence, primarily focusing on studies of Arabidopsis thaliana and rice (Oryza sativa). We also highlight recent progress in elucidating the interplay among various regulatory pathways, compare post-hypoxia reoxygenation between plants and animals and provide new perspectives for future studies.

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References

Zhou Y, Zhou D, Yu W, Shi L, Zhang Y, Lai Y . Phosphatidic acid modulates MPK3- and MPK6-mediated hypoxia signaling in Arabidopsis. Plant Cell. 2021; 34(2):889-909. PMC: 8824597. DOI: 10.1093/plcell/koab289. View

Ella E, Kawano N, Yamauchi Y, Tanaka K, Ismail A . Blocking ethylene perception enhances flooding tolerance in rice seedlings. Funct Plant Biol. 2020; 30(7):813-819. DOI: 10.1071/FP03049. View

Hsu F, Shih M . Plant defense after flooding. Plant Signal Behav. 2013; 8(11):e26922. PMC: 4091378. DOI: 10.4161/psb.26922. View

Shabala S, Shabala L, Barcelo J, Poschenrieder C . Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant Cell Environ. 2014; 37(10):2216-33. DOI: 10.1111/pce.12339. View

Bailey-Serres J, Voesenek L . Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol. 2008; 59:313-39. DOI: 10.1146/annurev.arplant.59.032607.092752. View

Liu X, Hajnoczky G . Altered fusion dynamics underlie unique morphological changes in mitochondria during hypoxia-reoxygenation stress. Cell Death Differ. 2011; 18(10):1561-72. PMC: 3172112. DOI: 10.1038/cdd.2011.13. View

Shabala S . Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol. 2011; 190(2):289-98. DOI: 10.1111/j.1469-8137.2010.03575.x. View

Tsuji H, Meguro N, Suzuki Y, Tsutsumi N, Hirai A, Nakazono M . Induction of mitochondrial aldehyde dehydrogenase by submergence facilitates oxidation of acetaldehyde during re-aeration in rice. FEBS Lett. 2003; 546(2-3):369-73. DOI: 10.1016/s0014-5793(03)00631-8. View

Li C, Jackson R . Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol. 2002; 282(2):C227-41. DOI: 10.1152/ajpcell.00112.2001. View

10.

Sagrillo-Fagundes L, Assuncao Salustiano E, Ruano R, Markus R, Vaillancourt C . Melatonin modulates autophagy and inflammation protecting human placental trophoblast from hypoxia/reoxygenation. J Pineal Res. 2018; 65(4):e12520. DOI: 10.1111/jpi.12520. View

11.

Xiao J, Zhu X, Kang B, Xu J, Wu L, Hong J . Hydrogen Sulfide Attenuates Myocardial Hypoxia-Reoxygenation Injury by Inhibiting Autophagy via mTOR Activation. Cell Physiol Biochem. 2015; 37(6):2444-53. DOI: 10.1159/000438597. View

12.

Tang H, Bi H, Liu B, Lou S, Song Y, Tong S . WRKY33 interacts with WRKY12 protein to up-regulate RAP2.2 during submergence induced hypoxia response in Arabidopsis thaliana. New Phytol. 2020; 229(1):106-125. DOI: 10.1111/nph.17020. View

13.

Doorly C, Graciet E . Lessons from Comparison of Hypoxia Signaling in Plants and Mammals. Plants (Basel). 2021; 10(5). PMC: 8157222. DOI: 10.3390/plants10050993. View

14.

Hartman S, Liu Z, van Veen H, Vicente J, Reinen E, Martopawiro S . Ethylene-mediated nitric oxide depletion pre-adapts plants to hypoxia stress. Nat Commun. 2019; 10(1):4020. PMC: 6728379. DOI: 10.1038/s41467-019-12045-4. View

15.

Singh S, Mackill D, Ismail A . Physiological basis of tolerance to complete submergence in rice involves genetic factors in addition to the SUB1 gene. AoB Plants. 2014; 6. PMC: 4243076. DOI: 10.1093/aobpla/plu060. View

16.

Kroemer G, Marino G, Levine B . Autophagy and the integrated stress response. Mol Cell. 2010; 40(2):280-93. PMC: 3127250. DOI: 10.1016/j.molcel.2010.09.023. View

17.

Voesenek L, Bailey-Serres J . Flood adaptive traits and processes: an overview. New Phytol. 2015; 206(1):57-73. DOI: 10.1111/nph.13209. View

18.

Tamang B, Fukao T . Plant Adaptation to Multiple Stresses during Submergence and Following Desubmergence. Int J Mol Sci. 2015; 16(12):30164-80. PMC: 4691168. DOI: 10.3390/ijms161226226. View

19.

Licausi F, Kosmacz M, Weits D, Giuntoli B, Giorgi F, Voesenek L . Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature. 2011; 479(7373):419-22. DOI: 10.1038/nature10536. View

20.

Holdsworth M, Vicente J, Sharma G, Abbas M, Zubrycka A . The plant N-degron pathways of ubiquitin-mediated proteolysis. J Integr Plant Biol. 2019; 62(1):70-89. DOI: 10.1111/jipb.12882. View