Deposition of a Cutin Apoplastic Barrier Separating Seed Maternal and Zygotic Tissues

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2019 Jul 12

PMID 31291882

Citations 8

Authors

Olivier Coen

Jing Lu

Wenjia Xu

Delphine De Vos

Christine Pechoux

Frederic Domergue

Damaris Grain

Loic Lepiniec

Enrico Magnani

Affiliations

Soon will be listed here.

Abstract

Background: In flowering plants, proper seed development is achieved through the constant interplay of fertilization products, embryo and endosperm, and maternal tissues. Communication between these compartments is supposed to be tightly regulated at their interfaces. Here, we characterize the deposition pattern of an apoplastic lipid barrier between the maternal inner integument and fertilization products in Arabidopsis thaliana seeds.

Results: We demonstrate that an apoplastic lipid barrier is first deposited by the ovule inner integument and undergoes de novo cutin deposition following central cell fertilization and relief of the FERTILIZATION INDEPENDENT SEED Polycomb group repressive mechanism. In addition, we show that the WIP zinc-finger TRANSPARENT TESTA 1 and the MADS-Box TRANSPARENT TESTA 16 transcription factors act maternally to promote its deposition by regulating cuticle biosynthetic pathways. Finally, mutant analyses indicate that this apoplastic barrier allows correct embryo sliding along the seed coat.

Conclusions: Our results revealed that the deposition of a cutin apoplastic barrier between seed maternal and zygotic tissues is part of the seed coat developmental program.

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References

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

Todd J, Post-Beittenmiller D, Jaworski J . KCS1 encodes a fatty acid elongase 3-ketoacyl-CoA synthase affecting wax biosynthesis in Arabidopsis thaliana. Plant J. 1999; 17(2):119-30. DOI: 10.1046/j.1365-313x.1999.00352.x. View

Millar A, Clemens S, Zachgo S, Giblin E, Taylor D, Kunst L . CUT1, an Arabidopsis gene required for cuticular wax biosynthesis and pollen fertility, encodes a very-long-chain fatty acid condensing enzyme. Plant Cell. 1999; 11(5):825-38. PMC: 144219. DOI: 10.1105/tpc.11.5.825. View

Sagasser M, Lu G, Hahlbrock K, Weisshaar B . A. thaliana TRANSPARENT TESTA 1 is involved in seed coat development and defines the WIP subfamily of plant zinc finger proteins. Genes Dev. 2002; 16(1):138-49. PMC: 155310. DOI: 10.1101/gad.212702. View

Nesi N, Debeaujon I, Jond C, Stewart A, Jenkins G, Caboche M . The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. Plant Cell. 2002; 14(10):2463-79. PMC: 151229. DOI: 10.1105/tpc.004127. View

Brunaud V, Balzergue S, Dubreucq B, Aubourg S, Samson F, Chauvin S . T-DNA integration into the Arabidopsis genome depends on sequences of pre-insertion sites. EMBO Rep. 2002; 3(12):1152-7. PMC: 1308325. DOI: 10.1093/embo-reports/kvf237. View

Debeaujon I, Nesi N, Perez P, Devic M, Grandjean O, Caboche M . Proanthocyanidin-accumulating cells in Arabidopsis testa: regulation of differentiation and role in seed development. Plant Cell. 2003; 15(11):2514-31. PMC: 280558. DOI: 10.1105/tpc.014043. View

Schnurr J, Shockey J, Browse J . The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. Plant Cell. 2004; 16(3):629-42. PMC: 385277. DOI: 10.1105/tpc.017608. View

Pighin J, Zheng H, Balakshin L, Goodman I, Western T, Jetter R . Plant cuticular lipid export requires an ABC transporter. Science. 2004; 306(5696):702-4. DOI: 10.1126/science.1102331. View

10.

Garcia D, Fitz Gerald J, Berger F . Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell. 2004; 17(1):52-60. PMC: 544489. DOI: 10.1105/tpc.104.027136. View

11.

Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C . Apoplastic polyesters in Arabidopsis surface tissues--a typical suberin and a particular cutin. Phytochemistry. 2005; 66(22):2643-58. DOI: 10.1016/j.phytochem.2005.09.027. View

12.

Kurdyukov S, Faust A, Nawrath C, Bar S, Voisin D, Efremova N . The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell. 2006; 18(2):321-39. PMC: 1356542. DOI: 10.1105/tpc.105.036079. View

13.

Baudry A, Caboche M, Lepiniec L . TT8 controls its own expression in a feedback regulation involving TTG1 and homologous MYB and bHLH factors, allowing a strong and cell-specific accumulation of flavonoids in Arabidopsis thaliana. Plant J. 2006; 46(5):768-79. DOI: 10.1111/j.1365-313X.2006.02733.x. View

14.

Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge J . The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell. 2007; 19(1):351-68. PMC: 1820950. DOI: 10.1105/tpc.106.048033. View

15.

Kannangara R, Branigan C, Liu Y, Penfield T, Rao V, Mouille G . The transcription factor WIN1/SHN1 regulates Cutin biosynthesis in Arabidopsis thaliana. Plant Cell. 2007; 19(4):1278-94. PMC: 1913754. DOI: 10.1105/tpc.106.047076. View

16.

Ukitsu H, Kuromori T, Toyooka K, Goto Y, Matsuoka K, Sakuradani E . Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant Cell Physiol. 2007; 48(11):1524-33. DOI: 10.1093/pcp/pcm139. View

17.

Li Y, Beisson F, Koo A, Molina I, Pollard M, Ohlrogge J . Identification of acyltransferases required for cutin biosynthesis and production of cutin with suberin-like monomers. Proc Natl Acad Sci U S A. 2007; 104(46):18339-44. PMC: 2084344. DOI: 10.1073/pnas.0706984104. View

18.

Tsuwamoto R, Fukuoka H, Takahata Y . GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J. 2007; 54(1):30-42. DOI: 10.1111/j.1365-313X.2007.03395.x. View

19.

Molina I, Ohlrogge J, Pollard M . Deposition and localization of lipid polyester in developing seeds of Brassica napus and Arabidopsis thaliana. Plant J. 2008; 53(3):437-49. DOI: 10.1111/j.1365-313X.2007.03348.x. View

20.

Raffaele S, Vailleau F, Leger A, Joubes J, Miersch O, Huard C . A MYB transcription factor regulates very-long-chain fatty acid biosynthesis for activation of the hypersensitive cell death response in Arabidopsis. Plant Cell. 2008; 20(3):752-67. PMC: 2329921. DOI: 10.1105/tpc.107.054858. View