Genetic and epigenetic control of transfer cell development in plants

a.
State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China
b.
School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK

More Information

Corresponding author: E-mail address: yuanj@genetics.ac.cn (Jing Yuan)

摘要

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Abstract: The inter-cellular translocation of nutrients in plant is mediated by highly specialized transfer cells (TCs). TCs share similar functional and structural features across a wide range of plant species, including location at plant exchange surfaces, rich in secondary wall ingrowths, facilitation of nutrient flow, and passage of select molecules. The fate of endosperm TCs is determined in the TC fate acquisition stage (TCF), before the structure features are formed in the TC differentiation stage (TCD). At present, the molecular basis of TC development in plants remains largely unknown. In this review, we summarize the important roles of the signaling molecules in different development phases, such as sugars in TCF and phytohormones in TCD, and discuss the genetic and epigenetic factors, including TC-specific genes and endogenous plant peptides, and their crosstalk with these signaling molecules as a complex regulatory network in regulation of TC development in plants.
- Transfer cells /
- Differentiation /
- Signals and genes network

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参考文献(79)

[1]	Andriunas, F.A., Zhang, H.M., Weber, H. et al. Plant J., 68 (2011),pp. 987-998
[2]	Andriunas, F.A., Zhang, H.M., Xia, X. et al. J. Exp. Bot., 63 (2012),pp. 695-709
[3]	Arun-Chinnappa, K.S., McCurdy, D.W. Front. Plant Sci., 6 (2015),p. 217
[4]	Barrero, C., Royo, J., Grijota-Martinez, C. et al. Planta, 229 (2009),pp. 235-247
[5]	Becker, H., Hueros, G., Maitz, M. et al.
[6]	Becraft, P.W. Cell fate specification in the cereal endosperm Semin. Cell Dev. Biol., 12 (2001),pp. 387-394
[7]	Berger, F. Endosperm: the crossroad of seed development Curr. Opin. Plant Biol., 6 (2003),pp. 42-50
[8]	Borisjuk, L., Weber, H., Panitz, R. et al. J. Plant Physiol., 147 (1995),pp. 203-218
[9]	Brown, R., Lemmon, B.E., Nguyen, H. et al. Sex. Plant Reprod., 12 (1999),pp. 32-42
[10]	Brown, R., Lemmon, B.E., Olsen, O.A. Endosperm development in barley: microtubule involvement in the morphogenetic pathway Plant Cell, 6 (1994),pp. 1241-1252
[11]	Brown, R., Lemmon, B.E., Olsen, O.A. J. Plant Res., 109 (1996),pp. 301-313
[12]	Brugiere, N., Humbert, S., Rizzo, N. et al. A member of the maize isopentenyl transferase gene family, Zea mays isopentenyl transferase 2 (ZmIPT2), encodes a cytokinin biosynthetic enzyme expressed during kernel development Plant Mol. Biol., 67 (2008),pp. 215-229
[13]	Brugiere, N., Jiao, S., Hantke, S. et al. Cytokinin oxidase gene expression in maize is localized to the vasculature, and is induced by cytokinins, abscisic acid, and abiotic stress Plant Physiol., 132 (2003),pp. 1228-1240
[14]	Cabrera, J., Bustos, R., Favery, B. et al. Mol. Plant Pathol., 15 (2013),pp. 627-636
[15]	Cabrera, J., Barcala, M., Fenoll, C. et al. Front. Plant Sci., 5 (2014),p. 107
[16]	Charlton, W.L., Keen, C.L., Merriman, C. et al. Development, 121 (1995),pp. 3089-3097
[17]	Cheng, W.H., Taliercio, E.W., Chourey, P.S. Proc. Natl. Acad. Sci. U. S. A., 96 (1999),pp. 10512-10517
[18]	Costa, L.M., Gutierrez-Marcos, J.F., Brutnell, T.P. et al. Development, 130 (2003),pp. 5009-5017
[19]	Costa, L.M., Gutierrez-Marcos, J.F., Dickinson, H.G. More than a yolk: the short life and complex times of the plant endosperm Trends Plant Sci., 9 (2004),pp. 507-514
[20]	Costa, L.M., Yuan, J., Rouster, J. et al. Maternal control of nutrient allocation in plant seeds by genomic imprinting Curr. Biol., 22 (2012),pp. 160-165
[21]	Davis, R.W., Smith, J.D., Cobb, B.G. A light and electron microscope investigation of the TC region of maize caryopses Can. J. Bot., 68 (1990),pp. 471-479
[22]	Dibley, S.J., Zhou, Y., Andriunas, F.A. et al. New Phytol., 182 (2009),pp. 863-877
[23]	Drea, S., Leader, D.J., Arnold, B.C. et al. Systematic spatial analysis of gene expression during wheat caryopsis development Plant Cell, 17 (2005),pp. 2172-2185
[24]	Felker, F.C., Shannon, J.C. Plant Physiol., 65 (1980),pp. 864-870
[25]	Forestan, C., Meda, S., Varotto, S. ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development Plant Physiol., 152 (2010),pp. 1373-1390
[26]	Fukuda, H. Signals that control plant vascular cell differentiation Nat. Rev. Mol. Cell Biol., 5 (2009),pp. 379-391
[27]	Gomez, E., Royo, J., Guo, Y. et al. Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1 Plant Cell, 14 (2002),pp. 598-610
[28]	Gomez, E., Royo, J., Muniz, L.M. et al. The maize transcription factor Myb-Related Protein-1 is a key regulator of the differentiation of transfer cells Plant Cell, 21 (2009),pp. 2022-2035
[29]	Guitton, A.-E., Page, D.R., Chambrier, P. et al. Development, 131 (2004),pp. 2971-2981
[30]	Gunning, B.E.S., Pate, J.S. “Transfer cells” plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—their occurrence, structure, and development Protoplasma, 68 (1969),pp. 107-133
[31]	Gutierrez-Marcos, J.F., Costa, L.M., Biderre-Petit, C. et al. Plant Cell, 16 (2004),pp. 1288-1301
[32]	Gutierrez-Marcos, J.F., Pennington, P.D., Costa, L.M. et al. Imprinting in the endosperm: a possible role in preventing wide hybridization Philos. Trans. R. Soc. Lond. B. Biol. Sci., 358 (2003),pp. 1105-1111
[33]	Huh, J.H., Bauer, M.J., Hsieh, T.F. et al. Endosperm gene imprinting and seed development Curr. Opin. Genet. Dev., 17 (2007),pp. 480-485
[34]	Haritatos, E., Medville, R., Turgeon, R. Planta, 211 (2000),pp. 105-111
[35]	Harrington, G.N., Nussbaumer, Y., Wang, X.-D. et al. Protoplasma, 200 (1997),pp. 35-50
[36]	Hueros, G., Royo, J., Maitz, M. et al. Evidence for factors regulating transfer cellTC-specific expression in maize endosperm Plant Mol. Biol., 41 (1999),pp. 141-153
[37]	Jones, M.G.K. Host-cell responses to endo-parasitic nematode attack: structure and function of giant-cells and syncytia Ann. Appl. Biol., 97 (1981),pp. 353-372
[38]	Kang, B.H., Xiong, Y., Williams, D.S. et al. Plant Physiol., 151 (2009),pp. 1366-1376
[39]	Kovalchuk, N., Smith, J., Pallotta, M. et al. Characterization of the wheat endosperm transfer cell -specific protein TaPR60 Plant Mol. Biol., 71 (2009),pp. 81-98
[40]	Lalonde, S., Boles, E., Hellmann, H. et al. The dual function of sugar carriers: transport and sugar sensing Plant Cell, 11 (1999),pp. 707-726
[41]	LeClere, S., Schmelz, E.A., Chourey, P.S. Cell wall invertase-deficient miniature1 kernels have altered phytohormone levels Phytochemistry, 69 (2008),pp. 692-699
[42]	LeClere, S., Schmelz, E.A., Chourey, P.S. Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels Plant Physiol., 153 (2010),pp. 306-318
[43]	Ligrone, R., Gambardella, R. The sporophyte-gametophyte junction in bryophytes Adv. Bryol., 3 (1988),pp. 225-274
[44]	Mahonen, A.P., Bishopp, A., Higuchi, M. et al. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development Science, 311 (2006),pp. 94-98
[45]	Mazarei, M., Lennon, K.A., Puthoff, D.P. et al. Expression of an Arabidopsisphos-phoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes Plant Mol. Biol., 53 (2003),pp. 513-530
[46]	McCurdy, D.W., Patrick, J.W., Offler, C.E. Wall ingrowth formation in transfer cells: novel examples of localized wall deposition in plant cells Curr. Opin. Plant Biol., 11 (2008),pp. 653-661
[47]	McDonald, C.R., Wang, H.L., Patrick, J.W. et al. Planta, 196 (1995),pp. 659-667
[48]	Mclaughlin, J.E., Boyer, J.S. Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems Ann. Bot., 94 (2004),pp. 75-86
[49]	Miller, M.E., Chourey, P.S. The maize invertase-deﬁcient miniature-1 seed mutation is associated with aberrant pedicel and endosperm development Plant Cell, 4 (1992),pp. 297-305
[50]	Mitchum, M.G., Wang, X., Wang, J. et al. Role of nematode peptides and other small molecules in plant parasitism Annu. Rev. Phytopathol., 50 (2012),pp. 175-195
[51]	Monjardino, P., Rocha, S., Tavares, A.C. et al. Protoplasma, 250 (2013),pp. 495-503
[52]	Muniz, L.M., Gomez, E., Guyon, V. et al. A PCR-based forward genetics screening, using expression domain specific markers, identifies mutants in endosperm transfer cell development Front. Plant Sci., 5 (2014),p. 158
[53]	Muniz, L.M., Royo, J., Gomez, E. et al. The maize transfer cell-speciﬁc type-A response regulator ZmTCRR-1 appears to be involved in intercellular signalling Plant J., 48 (2006),pp. 17-27
[54]	Muniz, L.M., Royo, J., Gomez, E. et al. Atypical response regulators expressed in the maize endosperm transfer cells link canonical two component systems and seed biology BMC Plant Biol., 10 (2010),pp. 84-100
[55]	Nguyen, S., McCurdy, David W. High-resolution confocal imaging of wall ingrowth deposition in plant transfer cells: semi-quantitative analysis of phloem parenchyma transfer cell development in leaf minor veins of Arabidopsis BMC Plant Biol., 15 (2015),p. 109
[56]	Offler, C.E., McCurdy, D.W., Patrick, J.W. et al. Transfer cells: cells specialized for a special purpose Annu. Rev. Plant Biol., 54 (2002),pp. 431-454
[57]	Offler, C.E., Liet, E., Sutton, E.G. Protoplasma, 200 (1997),pp. 51-64
[58]	Olsen, O.A. Endosperm development: cellularization and cell fate specification Annu. Rev. Plant Physiol. Plant Mol. Biol., 52 (2001),pp. 233-267
[59]	Olsen, O.A. Plant Cell, 16 (2004),pp. S214-S227
[60]	Olsen, O.A., Linnestad, C., Nichols, S.E. Developmental biology of the cereal endosperm Trends Plant Sci., 4 (1999),pp. 253-257
[61]	Patrick, J.W., Offler, C.E. Compartmentation of transport and transfer events in developing seeds J. Exp. Bot., 52 (2001),pp. 551-564
[62]	Radchuk, V.V., Borisjuk, L., Sreenivasulu, N. et al. Spatiotemporal profiling of starch biosynthesis and degradation in the developing barley grain Plant Physiol., 150 (2009),pp. 190-204
[63]	Rijavec, T., Kovac, M., Kladnik, A. et al. J. Integr. Plant Biol., 51 (2009),pp. 840-849
[64]	Royo, J., Gómez, E., Hueros, G.
[65]	Royo, J., Gómez, E., Sellam, O. et al. Front. Plant Sci., 5 (2014),p. 180
[66]	Sorensen, M.B., Chaudhury, A.M., Robert, H. et al. Polycomb group genes control pattern formation in plant seed Curr. Biol., 11 (2001),pp. 277-281
[67]	Tegeder, M., Wang, X.D., Frommer, W.B. et al. Plant J., 18 (1999),pp. 151-161
[68]	Thiel, J., Weier, D., Sreenivasulu, N. et al. Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: a microdissection-based transcriptome study of young barley grains Plant Physiol., 148 (2008),pp. 1436-1452
[69]	Thompson, R.D., Hueros, G., Becher, H. et al. Development and functions of seed transfer cells Plant Sci., 160 (2001),pp. 775-783
[70]	Wang, L., Ruan, Y. Plant Physiol., 160 (2012),pp. 777-787
[71]	Weber, H., Weschke, W. Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm TCs: a microdissection-based transcriptome study of young barley grains Plant Physiol., 148 (2008),pp. 1436-1452
[72]	Weschke, W., Panitz, R., Wang, Q. et al. Sucrose transport into barley seeds: molecular characterization of two transporters and implications for seed development and starch accumulation Plant J., 21 (2000),pp. 455-467
[73]	Wimmers, L.E., Turgeon, R. Planta, 186 (1991),pp. 2-12
[74]	Yang, H., Liu, X., Xin, M. et al. Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development Plant Cell, 28 (2016),pp. 629-645
[75]	Zhang, H., Helden, D.F., McCurdy, D.W. et al. Plant Cell Physiol., 56 (2015),pp. 1711-1720
[76]	Zhang, H., Talbot, M.J., McCurdy, D.W. et al. Calcium-dependent depletion zones in the cortical microtubule array coincide with sites of, but do not regulate, wall ingrowth papillae deposition in epidermal transfer cells J. Exp. Bot., 66 (2015),pp. 6021-6033
[77]	Zhang, H., Wheeler, S., Xia, X. et al. Plant Biol., 15 (2015),pp. 103-115
[78]	Zheng, Y., Wang, Z. Current opinions on endosperm TCs in maize Plant Cell Rep., 29 (2010),pp. 935-942
[79]	Zhou, Y., Andriunas, F., Offler, C.E. et al. New Phytol., 185 (2010),pp. 931-943