Development of Endosperm Transfer Cells in Barley

Overview

Journal Front Plant Sci

Date 2014 Apr 12

PMID 24723929

Citations 20

Authors

Johannes Thiel

Affiliations

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Abstract

Endosperm transfer cells (ETCs) are positioned at the intersection of maternal and filial tissues in seeds of cereals and represent a bottleneck for apoplasmic transport of assimilates into the endosperm. Endosperm cellularization starts at the maternal-filial boundary and generates the highly specialized ETCs. During differentiation barley ETCs develop characteristic flange-like wall ingrowths to facilitate effective nutrient transfer. A comprehensive morphological analysis depicted distinct developmental time points in establishment of transfer cell (TC) morphology and revealed intracellular changes possibly associated with cell wall metabolism. Embedded inside the grain, ETCs are barely accessible by manual preparation. To get tissue-specific information about ETC specification and differentiation, laser microdissection (LM)-based methods were used for transcript and metabolite profiling. Transcriptome analysis of ETCs at different developmental stages by microarrays indicated activated gene expression programs related to control of cell proliferation and cell shape, cell wall and carbohydrate metabolism reflecting the morphological changes during early ETC development. Transporter genes reveal distinct expression patterns suggesting a switch from active to passive modes of nutrient uptake with the onset of grain filling. Tissue-specific RNA-seq of the differentiating ETC region from the syncytial stage until functionality in nutrient transfer identified a high number of novel transcripts putatively involved in ETC differentiation. An essential role for two-component signaling (TCS) pathways in ETC development of barley emerged from this analysis. Correlative data provide evidence for abscisic acid and ethylene influences on ETC differentiation and hint at a crosstalk between hormone signal transduction and TCS phosphorelays. Collectively, the data expose a comprehensive view on ETC development, associated pathways and identified candidate genes for ETC specification.

Citing Articles

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References

Doan D, Linnestad C, Olsen O . Isolation of molecular markers from the barley endosperm coenocyte and the surrounding nucellus cell layers. Plant Mol Biol. 1996; 31(4):877-86. DOI: 10.1007/BF00019474. View

Muniz L, Royo J, Gomez E, Barrero C, Bergareche D, Hueros G . The maize transfer cell-specific type-A response regulator ZmTCRR-1 appears to be involved in intercellular signalling. Plant J. 2006; 48(1):17-27. DOI: 10.1111/j.1365-313X.2006.02848.x. View

Imamura A, Hanaki N, Nakamura A, Suzuki T, Taniguchi M, Kiba T . Compilation and characterization of Arabidopsis thaliana response regulators implicated in His-Asp phosphorelay signal transduction. Plant Cell Physiol. 1999; 40(7):733-42. DOI: 10.1093/oxfordjournals.pcp.a029600. View

Zhang W, Zhou Y, Dibley K, Tyerman S, Furbank R, Patrick J . Review: Nutrient loading of developing seeds. Funct Plant Biol. 2020; 34(4):314-331. DOI: 10.1071/FP06271. View

Tauris B, Borg S, Gregersen P, Holm P . A roadmap for zinc trafficking in the developing barley grain based on laser capture microdissection and gene expression profiling. J Exp Bot. 2009; 60(4):1333-47. PMC: 2657541. DOI: 10.1093/jxb/erp023. View

Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W . GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 2004; 136(1):2621-32. PMC: 523327. DOI: 10.1104/pp.104.046367. View

Schaller G, Kieber J, Shiu S . Two-component signaling elements and histidyl-aspartyl phosphorelays. Arabidopsis Book. 2012; 6:e0112. PMC: 3243373. DOI: 10.1199/tab.0112. View

Tran L, Urao T, Qin F, Maruyama K, Kakimoto T, Shinozaki K . Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci U S A. 2007; 104(51):20623-8. PMC: 2154481. DOI: 10.1073/pnas.0706547105. View

Sakakibara H, Suzuki M, Takei K, Deji A, Taniguchi M, Sugiyama T . A response-regulator homologue possibly involved in nitrogen signal transduction mediated by cytokinin in maize. Plant J. 1998; 14(3):337-44. DOI: 10.1046/j.1365-313x.1998.00134.x. View

10.

Thompson R, Hueros G, Maitz M . Development and functions of seed transfer cells. Plant Sci. 2001; 160(5):775-783. DOI: 10.1016/s0168-9452(01)00345-4. View

11.

Zheng Y, Wang Z . Contrast observation and investigation of wheat endosperm transfer cells and nucellar projection transfer cells. Plant Cell Rep. 2011; 30(7):1281-8. DOI: 10.1007/s00299-011-1039-5. View

12.

Riefler M, Novak O, Strnad M, Schmulling T . Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell. 2005; 18(1):40-54. PMC: 1323483. DOI: 10.1105/tpc.105.037796. View

13.

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

14.

Xue L, Zhang J, Xue H . Genome-wide analysis of the complex transcriptional networks of rice developing seeds. PLoS One. 2012; 7(2):e31081. PMC: 3281924. DOI: 10.1371/journal.pone.0031081. View

15.

Brown R, Lemmon B, Stone B, Olsen O . Cell wall (1-->3)- and (1-->3, 1-->4)-beta-glucans during early grain development in rice (Oryza sativa L.). Planta. 1997; 202(4):414-26. DOI: 10.1007/s004250050145. View

16.

Cheng W, Taliercio E, Chourey P . The Miniature1 Seed Locus of Maize Encodes a Cell Wall Invertase Required for Normal Development of Endosperm and Maternal Cells in the Pedicel. Plant Cell. 1996; 8(6):971-983. PMC: 161152. DOI: 10.1105/tpc.8.6.971. View

17.

Mizuno T . Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci Biotechnol Biochem. 2005; 69(12):2263-76. DOI: 10.1271/bbb.69.2263. View

18.

Talbot M, Offler C, McCurdy D . Transfer cell wall architecture: a contribution towards understanding localized wall deposition. Protoplasma. 2002; 219(3-4):197-209. DOI: 10.1007/s007090200021. View

19.

Chefdor F, Benedetti H, Depierreux C, Delmotte F, Morabito D, Carpin S . Osmotic stress sensing in Populus: components identification of a phosphorelay system. FEBS Lett. 2005; 580(1):77-81. DOI: 10.1016/j.febslet.2005.11.051. View

20.

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