Abstract
Endosperm transfer cells function as the nutrient transporter, antimicrobic barrier, and signal mediator between filial and maternal tissues. Sugar supply of maternal tissues, sugar demand of filial tissues, and requirement for defence against pathogens are three elemental factors inducing differentiation of endosperm transfer cells. Epigenetic factors, especially MEG1, moderate the key genetic factor ZmMRP-1 to activate endosperm transfer cell-specific genes that control the flange wall ingrowth formation and defensin-like protein secretion in maize. Auxin and cytokinin are primary hormones involved in development of maize endosperm transfer cells. Crosstalk between glucose and hormone signaling regulates endosperm transfer cell development via modifying ZmMRP-1 expression. This review summarizes the current knowledge on maize endosperm transfer cell development, and discusses its potential molecular mechanisms. It is expected to strengthen the theoretical basis for structural and functional optimization of endosperm transfer cells, and yield improvement of kernels in maize.
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References
Armengot L, Marquès-Bueno MM, Jaillais Y (2016) Regulation of polar auxin transport by protein and lipid kinases. J Exp Bot 67:4015–4037
Bai F, Daliberti M, Bagadion A, Xu M, Li Y, Baier J, Tseung CW, Evans MM, Settles AM (2016) Parent-of-origin-effect rough endosperm mutants in maize. Genetics 204:221–231
Barrero C, Muñiz LM, Gómez E, Hueros G, Royo J (2006) Molecular dissection of the interaction between the transcriptional activator ZmMRP-1 and the promoter of BETL-1. Plant Mol Biol 62:655–668
Barrero C, Royo J, Grijota-Martinez C, Faye C, Paul W, Sanz S, Steinbiss HH, Hueros G (2009) The promoter of ZmMRP-1, a maize transfer cell-specific transcription activator, is induced at solute exchange surfaces and responds to transport demands. Planta 229:235–247
Batista RA, Figueiredo DD, Santos-González J, Köhler C (2019) Auxin regulates endosperm cellularization in Arabidopsis. Genes Dev 33:466–476
Bergareche D, Royo J, Muñiz LM, Hueros G (2018) Cell wall invertase activity regulates the expression of the transfer cell-specific transcription factor ZmMRP-1. Planta 247:429–442
Bernardi J, Lanubile A, Li QB, Kumar D, Kladnik A, Cook SD, Ross JJ, Marocco A, Chourey PS (2012) Impaired auxin biosynthesis in the defective endosperm18 mutant is due to mutational loss of expression in the ZmYuc1 gene encoding endosperm-specific YUCCA1 protein in maize. Plant Physiol 160:1318–1328
Brugière N, Humbert S, Rizzo N, Bohn J, Habben JE (2008) A member of the maize isopentenyl transferase gene family, Zea mays isopentenyl transferase 2 (ZmIPT2), encodes a CK biosynthetic enzyme expressed during kernel development. Plant Mol Biol 67:215–229
Charlton WL, Keen CL, Merriman C, Lynch P, Greenland AJ, Dickinson HG (1995) Endosperm development in Zea mays; implication of gametic imprinting and paternal excess in regulation of transfer layer development. Development 121:3089–3097
Cheng WH, Taliercio EW, Chourey PS (1996) 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 8:971–983
Chettoor AM, Phillips AR, Coker CT, Dilkes B, Evans MM (2016) Maternal gametophyte effects on seed development in maize. Genetics 204:233–248
Chourey PS, Hueros G (2017) The basal endosperm transfer layer (BETL): gateway to the maize kernel. In: Larkins BA (ed) Maize Kernel Development. Springer, pp 56–67
Chu ZX, Ma Q, Lin YX, Tang XL, Zhou YQ, Zhu SW, Fan J, Cheng BJ (2011) Genome-wide identification, classification, and analysis of two-component signal system genes in maize. Genet Mol Res 10:3316–3330
Corso-Díaz X, Jaeger C, Chaitankar V, Swaroop A (2018) Epigenetic control of gene regulation during development and disease: a view from the retina. Prog Retin Eye Res 65:1–27
Costa LM, Yuan J, Rouster J, Paul W, Dickinson H, Gutierrez-Marcos JF (2012) Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr Biol 22:160–165
Dai D, Ma Z, Song R (2021) Maize endosperm development. J Integr Plant Biol 63:613–627
Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Front Plant Sci 5:493
Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JA (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104:14537–14542
Doll NM, Depège-Fargeix N, Rogowsky PM, Widiez T (2017) Signaling in early maize kernel development. Mol Plant 10(3):375–388
Forestan C, Meda S, Varotto S (2010) ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiol 152:1373–1390
Gómez E, Royo J, Guo Y, Thompson R, Hueros G (2002) Establishment of cereal endosperm expression domains: identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14:599–610
Gómez E, Royo J, Muñiz LM, Sellam O, Paul W, Gerentes D, Barrero C, López M, Perez P, Hueros G (2009) The maize transcription factor myb-related protein-1 is a key regulator of the differentiation of transfer cells. Plant Cell 21:2022–2035
Gutiérrez-Marcos JF, Costa LM, Biderre-Petit C, Khbaya B, O’Sullivan DM, Wormald M, Perez P, Dickinson HG (2004) Maternally expressed gene1 is a novel maize endosperm transfer cell-specific gene with a maternal parent-of-origin pattern of expression. Plant Cell 16:1288–1301
Gutiérrez-Marcos JF, Costa LM, Evans MMS (2006) Maternal gametophytic baseless1 is required for development of the central cell and early endosperm patterning in maize (Zea mays). Genetics 174:317–329
Hueros G, Varotto S, Salamini F, Thompson RD (1995) Molecular characterization of Bet1, a gene expressed in the endosperm transfer cells of maize. Plant Cell 7:747–757
Hueros G, Royo J, Maitz M, Salamini F, Thompson RD (1999) Evidence for factors regulating transfer cell-specific expression in maize endosperm. Plant Mol Biol 41:403–414
Kakani A, Peng Z (2011) ARR5 and ARR6 mediate tissue specific cross-talk between auxin and cytokinin in Arabidopsis. Am J Plant Sci 2:549–553
Kang BH, Xiong Y, Williams DS, Pozueta-Romero D, Chourey PS (2009) Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Physiol 151:1366–1376
Kim ED, Xiong Y, Pyo Y, Kim DH, Kang BH, Sung S (2017) Spatio-temporal analysis of coding and long noncoding transcripts during maize endosperm development. Sci Rep 7:3838
Knauss S, Rohrmeier T, Lehle L (2003) The auxin-induced maize gene ZmSAUR2 encodes a short-lived nuclear protein expressed in elongating tissues. J Biol Chem 278:23936–23943
LeCLere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiol 153:306–318
Li G, Wang D, Yang R, Logan K, Chen H, Zhang S, Skaggs MI, Lloyd A, Burnett WJ, Laurie JD, Hunter BG, Dannenhoffer JM, Larkins BA, Drews GN, Wang X, Yadegari R (2014) Temporal patterns of gene expression in developing maize endosperm identified through transcriptome sequencing. Proc Natl Acad Sci U S A 111:7582–7587
Liu Y, Jiang H, Chen W, Qian Y, Ma Q, Cheng B, Zhu S (2011) Genome-wide analysis of the auxin response factor (ARF) gene family in maize (Zea mays). Plant Growth Regul 63:225–234
Lur HS, Setter TL (1993) Role of auxin in maize endosperm development (timing of nuclear DNA endoreduplication, zein expression, and cytokinin). Plant Physiol 103:273–280
Ma C, Li B, Wang L, Xu ML, Lizhu E, Jin H, Wang Z, Ye JR (2019) Characterization of phytohormone and transcriptome reprogramming profiles during maize early kernel development. BMC Plant Biol 19:197
Maitz M, Santandrea G, Zhang Z, Lal S, Hannah LC, Salamini F, Thompson RD (2000) rgf1, a mutation reducing grain filling in maize through effects on basal endosperm and pedicel development. Plant J 23:29–42
Majda M, Robert S (2018) The role of auxin in cell wall expansion. Int J Mol Sci 19:951
Mir R, Aranda LZ, Biaocchi T, Luo A, Sylvester AW, Rasmussen CG (2017) A DII-based auxin reporter uncovers low auxin signaling during telophase and early G1. Plant Physiol 173:863–871
Monjardino P, Rocha S, Tavares AC, Fernandes R, Sampaio P, Salema R, da Câmara MA (2013) Development of flange and reticulate wall ingrowths in maize (Zea mays L.) endosperm transfer cells. Protoplasma 250:495–503
Muñiz LM, Royo J, Gómez E, Barrero C, Bergareche D, Hueros G (2006) The maize transfer cell-specific type-A response regulator ZmTCRR-1 appears to be involved in intercellular signaling. Plant J 48:17–27
Muñiz LM, Royo J, Gomez E, Baudot G, Paul W, Hueros G (2010) Atypical response regulators expressed in the maize endosperm transfer cells link canonical two component systems and seed biology. BMC Plant Biol 10:84
Offler CE, Patrick JW (2020) Transfer cells: what regulates the development of their intricate wall labyrinths? New Phytol 228:427–444
Offler CE, McCurdy DW, Patrick JW, Talbot MJ (2003) Transfer cells: cells specialized for a special purpose. Annu Rev Plant Biol 54:431–454
Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267
Olsen OA (2020) The modular control of cereal endosperm development. Trends Plant Sci 25(3):279–290
Opsahl-Ferstad HG, Le Deunff E, Dumas C, Rogowsky PM (1997) ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J 12:235–246
Panda BB, Sekhar S, Dash SK, Behera L, Shaw BP (2018) Biochemical and molecular characterisation of exogenous cytokinin application on grain filling in rice. BMC Plant Biol 18:89
Rijavec T, Jain M, Dermastia M, Chourey PS (2011) Spatial and temporal profiles of cytokinin biosynthesis and accumulation in developing caryopses of maize. Ann Bot 107:1235–1245
Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283:1541–1544
Royo J, Gómez E, Barrero C, Muñiz LM, Sanz Y, Hueros G (2009) Transcriptional activation of the maize endosperm transfer cell-specific gene BETL1 by ZmMRP-1 is enhanced by two C2H2 zinc finger-containing proteins. Planta 230:807–818
Salehin M, Bagchi R, Estelle M (2015) SCFTIR1/AFB-based auxin perception: mechanism and role in plant growth and development. Plant Cell 27:9–19
Semeradova H, Montesinos JC, Benkova E (2020) All roads lead to auxin: post-translational regulation of auxin transport by multiple hormonal pathways. Plant Comm 1:100048
Serna A, Maitz M, O’Connell T, Santandrea G, Thevissen K, Tienens K, Hueros G, Faleri C, Cai G, Lottspeich F, Thompson RD (2001) Maize endosperm secretes a novel antifungal protein into adjacent maternal tissue. Plant J 25:687–698
Skalický V, Kubeš M, Napier R, Novák O (2018) Auxins and cytokinins-the role of subcellular organization on homeostasis. Int J Mol Sci 19:3115
Sosso D, Luo D, Li Q-B, Sasse J, Yang J, Gendrot G, Suzuki M, Koch KE, McCarty DR, Chourey PS, Rogowsky PM, Ross-Ibarra J, Yang B, Frommer WB (2015) Seed filling in domesticated maize and rice depends on SWEET-mediated hexose transport. Nat Genet 47:1489–1493
Strader LC, Zhao Y (2016) Auxin perception and downstream events. Curr Opin Plant Biol 33:8–14
Talbot MJ, Offler CE, McCurdy DW (2002) Transfer cell wall architecture: a contribution towards understanding localized wall deposition. Protoplasma 219:197–209
Thiel J (2014) Development of endosperm transfer cells in barley. Front Plant Sci 5:108
Thiel J, Hollmann J, Rutten T, Weber H, Scholz U, Weschke W (2012) 454 Transcriptome sequencing suggests a role for two-component signaling in cellularization and differentiation of barley endosperm transfer cells. PLoS ONE 7:e41867
Thompson RD, Hueros G, Becker H, Maitz M (2001) Development and functions of seed transfer cells. Plant Sci 160:775–783
Tombuloglu H, Aydin M, Filiz E (2016) Comparative analysis of embryo surrounding region (Esr-6) genes in Turkish maize varieties: sequencing and modeling. Braz J Bot 39:287–293
Vankova R (2014) Cytokinin regulation of plant growth and stress responses. In: Tran LS, Pal S (eds) Phytohormones: a window to metabolism, signaling and biotechnological applications. Springer, New York, NY, pp 55–79
Velasquez SM, Barbez E, Kleine-Vehn J, Estevez JM (2016) Auxin and cellular elongation. Plant Physiol 170:1206–1215
Wang Y, Deng D, Bian Y, Lv Y, Xie Q (2010) Genome-wide analysis of primary auxin-responsive Aux/IAA gene family in maize (Zea mays. L.). Mol Biol Rep 37:3991–4001
Xin M, Yang R, Li G, Chen H, Laurie J, Ma C, Wang D, Yao Y, Larkins BA, Sun Q, Yadegari R, Wang X, Ni Z (2013) Dynamic expression of imprinted genes associates with maternally controlled nutrient allocation during maize endosperm development. Plant Cell 25:3212–3227
Xiong Y, Mei W, Kim ED, Mukherjee K, Hassanein H, Barbazuk WB, Sung S, Kolaczkowski B, Kang BH (2014) Adaptive expansion of the maize maternally expressed gene (Meg) family involves changes in expression patterns and protein secondary structures of its members. BMC Plant Biol 14:204
Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusová H, Wang W, Jones AM, Friml J, Patterson SE, Bleecker AB, Yang Z (2014) Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science 343:1025–1028
Yang H, Liu X, Xin M, Du J, Hu Z, Peng H, Rossi V, Sun Q, Ni Z, Yao Y (2016) Genome-wide mapping of targets of maize histone deacetylase HDA101 reveals its function and regulatory mechanism during seed development. Plant Cell 28:629–645
Yi F, Gu W, Chen J, Song N, Gao X, Zhang X, Zhou Y, Ma Y, Song W, Zhao H, Esteban E, Pasha A, Provart NJ, Lai J (2019) High temporal-resolution transcriptional landscape of early maize seed development. Plant Cell 31:974–992
Yuan J, Bateman P, Gutierrez-Marcos J (2016) Genetic and epigenetic control of transfer cell development in plants. J Genet Genomics 43:533–539
Zhan J, Thakare D, Ma C, Lloyd A, Nixon NM, Arakaki AM, Burnett WJ, Logan KO, Wang D, Wang X, Drews GN, Yadegari R (2015) RNA sequencing of laser-capture microdissected compartments of the maize kernel identifies regulatory modules associated with endosperm cell differentiation. Plant Cell 27:513–531
Zhang HM, Colyvas K, Patrick JW, Offler CE (2017) A Ca2+-dependent remodelled actin network directs vesicle trafficking to build wall ingrowth papillae in transfer cells. J Exp Bot 6868:4749–4764
Zheng Y, Wang Z (2014) Protein accumulation in aleurone cells, sub-aleurone cells and the center starch endosperm of cereals. Plant Cell Rep 33:1607–1615
Zheng Y, Wang Z, Gu Y (2014) Development and function of caryopsis transport tissues in maize, sorghum and wheat. Plant Cell Rep 33:1023–1031
Zheng Y, Yang J, Wang Z, Gu Y (2015) Structure characteristics and function of maize endosperm transfer cells. Braz J Bot 38:669–678
Zhou JJ, Luo J (2018) The PIN-FORMED auxin efflux carriers in plants. Int J Mol Sci 19:2759
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Thanks a lot for the fund support from Anqing Normal University.
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This work was supported by the Doctoral Startup Fund of Scientific Research from Anqing Normal University (Grant No.150002033).
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Zheng, Y. Molecular mechanisms of maize endosperm transfer cell development. Plant Cell Rep 41, 1171–1180 (2022). https://doi.org/10.1007/s00299-021-02807-0
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DOI: https://doi.org/10.1007/s00299-021-02807-0