LIP5, a MVB Biogenesis Regulator, is Required for Rice Growth

Overview

Journal Front Plant Sci

Date 2023 Feb 3

PMID 36733718

Authors

Mengxue Wang

Shuwei Luo

Baofang Fan

Cheng Zhu

Zhixiang Chen

Affiliations

Soon will be listed here.

Abstract

LYST-INTERACTING PROTEIN5 (LIP5) is a conserved regulator of multivesicular body (MVB) biogenesis in eukaryotes. In Arabidopsis, AtLIP5 is a target of stress-responsive MITOGEN-ACTIVATED PROTEIN KINASE3 and 6 and mediates stress-induced MVB biogenesis to promote stress responses. However, Arabidopsis knockout mutants are normal in growth and development. Here we report that rice gene could fully restore both the disease resistance and salt tolerance of the Arabidopsis mutant plants to the wild-type levels. Unlike Arabidopsis mutants, rice mutants were severely stunted, developed necrotic lesions and all died before flowering. Unlike in Arabidopsis, LIP5 regulated endocytosis under both stress and normal conditions in rice. These findings indicate that there is strong evolutionary divergence among different plants in the role of the conserved LIP5-regulated MVB pathway in normal plant growth.

Citing Articles

Vesicle trafficking in rice: too little is known.

Zhu X, Yin J, Guo H, Wang Y, Ma B Front Plant Sci. 2023; 14:1263966.

PMID: 37790794 PMC: 10543891. DOI: 10.3389/fpls.2023.1263966.

References

Stahl P, Alejandro Barbieri M . Multivesicular bodies and multivesicular endosomes: the "ins and outs" of endosomal traffic. Sci STKE. 2002; 2002(141):pe32. DOI: 10.1126/stke.2002.141.pe32. View

Lai Z, Wang F, Zheng Z, Fan B, Chen Z . A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J. 2011; 66(6):953-68. DOI: 10.1111/j.1365-313X.2011.04553.x. View

Vild C, Li Y, Guo E, Liu Y, Xu Z . A novel mechanism of regulating the ATPase VPS4 by its cofactor LIP5 and the endosomal sorting complex required for transport (ESCRT)-III protein CHMP5. J Biol Chem. 2015; 290(11):7291-303. PMC: 4358147. DOI: 10.1074/jbc.M114.616730. View

Masclaux-Daubresse C, Clement G, Anne P, Routaboul J, Guiboileau A, Soulay F . Stitching together the Multiple Dimensions of Autophagy Using Metabolomics and Transcriptomics Reveals Impacts on Metabolism, Development, and Plant Responses to the Environment in Arabidopsis. Plant Cell. 2014; 26(5):1857-1877. PMC: 4079355. DOI: 10.1105/tpc.114.124677. View

Xia Z, Huo Y, Wei Y, Chen Q, Xu Z, Zhang W . The Arabidopsis LYST INTERACTING PROTEIN 5 Acts in Regulating Abscisic Acid Signaling and Drought Response. Front Plant Sci. 2016; 7:758. PMC: 4887465. DOI: 10.3389/fpls.2016.00758. View

Guo E, Xu Z . Distinct mechanisms of recognizing endosomal sorting complex required for transport III (ESCRT-III) protein IST1 by different microtubule interacting and trafficking (MIT) domains. J Biol Chem. 2015; 290(13):8396-408. PMC: 4375492. DOI: 10.1074/jbc.M114.607903. View

Xu L, Zhao H, Ruan W, Deng M, Wang F, Peng J . ABNORMAL INFLORESCENCE MERISTEM1 Functions in Salicylic Acid Biosynthesis to Maintain Proper Reactive Oxygen Species Levels for Root Meristem Activity in Rice. Plant Cell. 2017; 29(3):560-574. PMC: 5385951. DOI: 10.1105/tpc.16.00665. View

Wang F, Yang Y, Wang Z, Zhou J, Fan B, Chen Z . A Critical Role of Lyst-Interacting Protein5, a Positive Regulator of Multivesicular Body Biogenesis, in Plant Responses to Heat and Salt Stresses. Plant Physiol. 2015; 169(1):497-511. PMC: 4577394. DOI: 10.1104/pp.15.00518. View

Fink A . Chaperone-mediated protein folding. Physiol Rev. 1999; 79(2):425-49. DOI: 10.1152/physrev.1999.79.2.425. View

10.

Izumi M, Nakamura S . Chloroplast Protein Turnover: The Influence of Extraplastidic Processes, Including Autophagy. Int J Mol Sci. 2018; 19(3). PMC: 5877689. DOI: 10.3390/ijms19030828. View

11.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

12.

Wang F, Shang Y, Fan B, Yu J, Chen Z . Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense. PLoS Pathog. 2014; 10(7):e1004243. PMC: 4092137. DOI: 10.1371/journal.ppat.1004243. View

13.

McLoughlin F, Marshall R, Ding X, Chatt E, Kirkpatrick L, Augustine R . Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize. Plant Cell. 2020; 32(9):2699-2724. PMC: 7474275. DOI: 10.1105/tpc.20.00226. View

14.

Liu X, Zhou X, Li K, Wang D, Ding Y, Liu X . A simple and efficient cloning system for CRISPR/Cas9-mediated genome editing in rice. PeerJ. 2020; 8:e8491. PMC: 6995270. DOI: 10.7717/peerj.8491. View

15.

Li X, Wang Z, Fu Y, Cheng X, Zhang Y, Fan B . Two ubiquitin-associated ER proteins interact with COPT copper transporters and modulate their accumulation. Plant Physiol. 2021; 187(4):2469-2484. PMC: 8644684. DOI: 10.1093/plphys/kiab381. View

16.

Luo S, Li X, Zhang Y, Fu Y, Fan B, Zhu C . Cargo Recognition and Function of Selective Autophagy Receptors in Plants. Int J Mol Sci. 2021; 22(3). PMC: 7864022. DOI: 10.3390/ijms22031013. View

17.

Hiei Y, Ohta S, Komari T, Kumashiro T . Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 1994; 6(2):271-82. DOI: 10.1046/j.1365-313x.1994.6020271.x. View

18.

Spitzer C, Reyes F, Buono R, Sliwinski M, Haas T, Otegui M . The ESCRT-related CHMP1A and B proteins mediate multivesicular body sorting of auxin carriers in Arabidopsis and are required for plant development. Plant Cell. 2009; 21(3):749-66. PMC: 2671707. DOI: 10.1105/tpc.108.064865. View

19.

Have M, Luo J, Tellier F, Balliau T, Cueff G, Chardon F . Proteomic and lipidomic analyses of the Arabidopsis atg5 autophagy mutant reveal major changes in endoplasmic reticulum and peroxisome metabolisms and in lipid composition. New Phytol. 2019; 223(3):1461-1477. DOI: 10.1111/nph.15913. View

20.

Kurusu T, Koyano T, Hanamata S, Kubo T, Noguchi Y, Yagi C . OsATG7 is required for autophagy-dependent lipid metabolism in rice postmeiotic anther development. Autophagy. 2014; 10(5):878-88. PMC: 5119067. DOI: 10.4161/auto.28279. View