GDSL-domain Proteins Have Key Roles in Suberin Polymerization and Degradation

Overview

Journal Nat Plants

Specialties Biology
Genetics

Date 2021 Mar 9

PMID 33686223

Citations 54

Authors

Robertas Ursache

Cristovao de Jesus Vieira Teixeira

Valerie Denervaud Tendon

Kay Gully

Damien De Bellis

Emanuel Schmid-Siegert

Tonni Grube Andersen

Vinay Shekhar

Sandra Calderon

Sylvain Pradervand

Christiane Nawrath

Niko Geldner

Joop E M Vermeer

Affiliations

Soon will be listed here.

Abstract

Plant roots acquire nutrients and water while managing interactions with the soil microbiota. The root endodermis provides an extracellular diffusion barrier through a network of lignified cell walls called Casparian strips, supported by subsequent formation of suberin lamellae. Whereas lignification is thought to be irreversible, suberin lamellae display plasticity, which is crucial for root adaptative responses. Although suberin is a major plant polymer, fundamental aspects of its biosynthesis and turnover have remained obscure. Plants shape their root system via lateral root formation, an auxin-induced process requiring local breaking and re-sealing of endodermal lignin and suberin barriers. Here, we show that differentiated endodermal cells have a specific, auxin-mediated transcriptional response dominated by cell wall remodelling genes. We identified two sets of auxin-regulated GDSL lipases. One is required for suberin synthesis, while the other can drive suberin degradation. These enzymes have key roles in suberization, driving root suberin plasticity.

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References

Castrillo G, Teixeira P, Herrera Paredes S, Law T, de Lorenzo L, Feltcher M . Root microbiota drive direct integration of phosphate stress and immunity. Nature. 2017; 543(7646):513-518. PMC: 5364063. DOI: 10.1038/nature21417. View

Duran P, Thiergart T, Garrido-Oter R, Agler M, Kemen E, Schulze-Lefert P . Microbial Interkingdom Interactions in Roots Promote Arabidopsis Survival. Cell. 2018; 175(4):973-983.e14. PMC: 6218654. DOI: 10.1016/j.cell.2018.10.020. View

Hassani M, Duran P, Hacquard S . Microbial interactions within the plant holobiont. Microbiome. 2018; 6(1):58. PMC: 5870681. DOI: 10.1186/s40168-018-0445-0. View

Banda J, Bellande K, von Wangenheim D, Goh T, Guyomarch S, Laplaze L . Lateral Root Formation in Arabidopsis: A Well-Ordered LRexit. Trends Plant Sci. 2019; 24(9):826-839. DOI: 10.1016/j.tplants.2019.06.015. View

Stoeckle D, Thellmann M, Vermeer J . Breakout-lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol. 2017; 41:67-72. DOI: 10.1016/j.pbi.2017.09.005. View

Barberon M, Vermeer J, De Bellis D, Wang P, Naseer S, Andersen T . Adaptation of Root Function by Nutrient-Induced Plasticity of Endodermal Differentiation. Cell. 2016; 164(3):447-59. DOI: 10.1016/j.cell.2015.12.021. View

Li B, Kamiya T, Kalmbach L, Yamagami M, Yamaguchi K, Shigenobu S . Role of LOTR1 in Nutrient Transport through Organization of Spatial Distribution of Root Endodermal Barriers. Curr Biol. 2017; 27(5):758-765. DOI: 10.1016/j.cub.2017.01.030. View

Yadav V, Molina I, Ranathunge K, Queralta Castillo I, Rothstein S, Reed J . ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. Plant Cell. 2014; 26(9):3569-88. PMC: 4213157. DOI: 10.1105/tpc.114.129049. View

Vermeer J, von Wangenheim D, Barberon M, Lee Y, Stelzer E, Maizel A . A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science. 2014; 343(6167):178-83. DOI: 10.1126/science.1245871. View

10.

Tian Q, Uhlir N, Reed J . Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell. 2002; 14(2):301-19. PMC: 152914. DOI: 10.1105/tpc.010283. View

11.

Fukaki H, Tameda S, Masuda H, Tasaka M . Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. Plant J. 2002; 29(2):153-68. DOI: 10.1046/j.0960-7412.2001.01201.x. View

12.

Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y . The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol. 2008; 10(8):946-54. DOI: 10.1038/ncb1754. View

13.

Lewis D, Olex A, Lundy S, Turkett W, Fetrow J, Muday G . A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. Plant Cell. 2013; 25(9):3329-46. PMC: 3809535. DOI: 10.1105/tpc.113.114868. View

14.

Voss U, Wilson M, Kenobi K, Gould P, Robertson F, Peer W . The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun. 2015; 6:7641. PMC: 4506504. DOI: 10.1038/ncomms8641. View

15.

Bakan B, Marion D . Assembly of the Cutin Polyester: From Cells to Extracellular Cell Walls. Plants (Basel). 2017; 6(4). PMC: 5750633. DOI: 10.3390/plants6040057. View

16.

Girard A, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J . Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell. 2012; 24(7):3119-34. PMC: 3426136. DOI: 10.1105/tpc.112.101055. View

17.

Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N . Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci U S A. 2012; 109(25):10101-6. PMC: 3382560. DOI: 10.1073/pnas.1205726109. View

18.

Philippe G, Gaillard C, Petit J, Geneix N, Dalgalarrondo M, Bres C . Ester Cross-Link Profiling of the Cutin Polymer of Wild-Type and Cutin Synthase Tomato Mutants Highlights Different Mechanisms of Polymerization. Plant Physiol. 2015; 170(2):807-20. PMC: 4734573. DOI: 10.1104/pp.15.01620. View

19.

Yeats T, Martin L, Viart H, Isaacson T, He Y, Zhao L . The identification of cutin synthase: formation of the plant polyester cutin. Nat Chem Biol. 2012; 8(7):609-11. PMC: 3434877. DOI: 10.1038/nchembio.960. View

20.

Berhin A, De Bellis D, Franke R, Buono R, Nowack M, Nawrath C . The Root Cap Cuticle: A Cell Wall Structure for Seedling Establishment and Lateral Root Formation. Cell. 2019; 176(6):1367-1378.e8. DOI: 10.1016/j.cell.2019.01.005. View