A Ca2+-dependent Remodelled Actin Network Directs Vesicle Trafficking to Build Wall Ingrowth Papillae in Transfer Cells

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2017 Oct 20

PMID 29048561

Citations 3

Authors

Hui-Ming Zhang

Kim Colyvas

John W Patrick

Christina E Offler

Affiliations

Soon will be listed here.

Abstract

The transport function of transfer cells is conferred by an enlarged plasma membrane area, enriched in nutrient transporters, that is supported on a scaffold of wall ingrowth (WI) papillae. Polarized plumes of elevated cytosolic Ca2+ define loci at which WI papillae form in developing adaxial epidermal transfer cells of Vicia faba cotyledons that are induced to trans-differentiate when the cotyledons are placed on culture medium. We evaluated the hypothesis that vesicle trafficking along a Ca2+-regulated remodelled actin network is the mechanism that underpins this outcome. Polarized to the outer periclinal cytoplasm, a Ca2+-dependent remodelling of long actin bundles into short, thin bundles was found to be essential for assembling WI papillae but not the underlying uniform wall layer. The remodelled actin network directed polarized vesicle trafficking to sites of WI papillae construction, and a pharmacological study indicated that both exo- and endocytosis contributed to assembly of the papillae. Potential candidates responsible for the Ca2+-dependent actin remodelling, along with those underpinning polarized exo- and endocyotosis, were identified in a transcriptome RNAseq database generated from the trans-differentiating epidermal cells. Of most significance, endocytosis was controlled by up-regulated expression of a dynamin-like isoform. How a cycle of localized exo- and endocytosis, regulated by Ca2+-dependent actin remodelling, assembles WI papillae is discussed.

Citing Articles

Enzymes contributing to the hydrogen peroxide signal dynamics that regulate wall labyrinth formation in transfer cells.

Xia X, Zhang H, Offler C, Patrick J J Exp Bot. 2019; 71(1):219-233.

PMID: 31587068 PMC: 6913738. DOI: 10.1093/jxb/erz443.

Ethylene and hydrogen peroxide regulate formation of a sterol-enriched domain essential for wall labyrinth assembly in transfer cells.

Zhang H, Devine L, Xia X, Offler C, Patrick J J Exp Bot. 2019; 70(5):1469-1482.

PMID: 30649402 PMC: 6411373. DOI: 10.1093/jxb/erz003.

Transcript Profiling Identifies Gene Cohorts Controlled by Each Signal Regulating -Differentiation of Epidermal Cells of Cotyledons to a Transfer Cell Phenotype.

Zhang H, Wheeler S, Xia X, Colyvas K, Offler C, Patrick J Front Plant Sci. 2017; 8:2021.

PMID: 29234338 PMC: 5712318. DOI: 10.3389/fpls.2017.02021.

References

Li X, Li J, Wang W, Chen N, Ma T, Xi Y . ARP2/3 complex-mediated actin dynamics is required for hydrogen peroxide-induced stomatal closure in Arabidopsis. Plant Cell Environ. 2013; 37(7):1548-60. DOI: 10.1111/pce.12259. View

Wardini T, Wang X, Offler C, Patrick J . Induction of wall ingrowths of transfer cells occurs rapidly and depends upon gene expression in cotyledons of developing Vicia faba seeds. Protoplasma. 2007; 231(1-2):15-23. DOI: 10.1007/s00709-007-0244-0. View

Samaj J, Peters M, Volkmann D, Baluska F . Effects of myosin ATPase inhibitor 2,3-butanedione 2-monoxime on distributions of myosins, F-actin, microtubules, and cortical endoplasmic reticulum in maize root apices. Plant Cell Physiol. 2000; 41(5):571-82. DOI: 10.1093/pcp/41.5.571. View

Huang S, Qu X, Zhang R . Plant villins: versatile actin regulatory proteins. J Integr Plant Biol. 2014; 57(1):40-9. DOI: 10.1111/jipb.12293. View

Talbot M, Franceschi V, McCurdy D, Offler C . Wall ingrowth architecture in epidermal transfer cells of Vicia faba cotyledons. Protoplasma. 2001; 215(1-4):191-203. DOI: 10.1007/BF01280314. View

Offler C, McCurdy D, Patrick J, Talbot M . Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol. 2003; 54:431-54. DOI: 10.1146/annurev.arplant.54.031902.134812. View

Dibley S, Zhou Y, Andriunas F, Talbot M, Offler C, Patrick J . Early gene expression programs accompanying trans-differentiation of epidermal cells of Vicia faba cotyledons into transfer cells. New Phytol. 2009; 182(4):863-877. DOI: 10.1111/j.1469-8137.2009.02822.x. View

Szymanski D, Cosgrove D . Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Curr Biol. 2009; 19(17):R800-11. DOI: 10.1016/j.cub.2009.07.056. View

Zhang H, Imtiaz M, Laver D, McCurdy D, Offler C, van Helden D . Polarized and persistent Ca²⁺ plumes define loci for formation of wall ingrowth papillae in transfer cells. J Exp Bot. 2014; 66(5):1179-90. PMC: 4339585. DOI: 10.1093/jxb/eru460. View

10.

van de Meene A, Doblin M, Bacic A . The plant secretory pathway seen through the lens of the cell wall. Protoplasma. 2016; 254(1):75-94. DOI: 10.1007/s00709-016-0952-4. View

11.

Spector I, Shochet N, Kashman Y, Groweiss A . Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science. 1983; 219(4584):493-5. DOI: 10.1126/science.6681676. View

12.

Martiniere A, Gayral P, Hawes C, Runions J . Building bridges: formin1 of Arabidopsis forms a connection between the cell wall and the actin cytoskeleton. Plant J. 2011; 66(2):354-65. DOI: 10.1111/j.1365-313X.2011.04497.x. View

13.

Li J, Blanchoin L, Staiger C . Signaling to actin stochastic dynamics. Annu Rev Plant Biol. 2014; 66:415-40. DOI: 10.1146/annurev-arplant-050213-040327. View

14.

Paez Valencia J, Goodman K, Otegui M . Endocytosis and Endosomal Trafficking in Plants. Annu Rev Plant Biol. 2016; 67:309-35. DOI: 10.1146/annurev-arplant-043015-112242. View

15.

Ketelaar T, Galway M, Mulder B, Emons A . Rates of exocytosis and endocytosis in Arabidopsis root hairs and pollen tubes. J Microsc. 2008; 231(2):265-73. DOI: 10.1111/j.1365-2818.2008.02031.x. View

16.

Haraguchi T, Tominaga M, Nakano A, Yamamoto K, Ito K . Myosin XI-I is Mechanically and Enzymatically Unique Among Class-XI Myosins in Arabidopsis. Plant Cell Physiol. 2016; 57(8):1732-43. DOI: 10.1093/pcp/pcw097. View

17.

Spiro D, Boll W, Kirchhausen T, Wessling-Resnick M . Wortmannin alters the transferrin receptor endocytic pathway in vivo and in vitro. Mol Biol Cell. 1996; 7(3):355-67. PMC: 275889. DOI: 10.1091/mbc.7.3.355. View

18.

Yoo C, Quan L, Cannon A, Wen J, Blancaflor E . AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J. 2011; 69(6):1064-76. DOI: 10.1111/j.1365-313X.2011.04856.x. View

19.

Smertenko A, Deeks M, Hussey P . Strategies of actin reorganisation in plant cells. J Cell Sci. 2010; 123(Pt 17):3019-28. DOI: 10.1242/jcs.071126. View

20.

Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R . Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ. 2013; 37(5):1250-8. DOI: 10.1111/pce.12231. View