Abstract
The major tissues of the cereal endosperm are the starchy endosperm (SE) in the inner and the aleurone layer (AL) at the outer periphery. The fates of the cells that comprise these tissues are determined according to positional information; however, our understanding of the underlying molecular mechanisms remains limited. Here, we conducted a high-resolution spatiotemporal analysis of the rice endosperm transcriptome during early cellularization. In rice, endosperm cellularization proceeds in a concentric pattern from a primary alveolus cell layer, such that developmental progression can be defined by the number of cell layers. Using laser-capture microdissection to obtain precise tissue sections, transcriptomic changes were followed through five histologically defined stages of cellularization from the syncytial to 3-cell layer (3 L) stage. In addition, transcriptomes were compared between the inner and the outermost peripheral cell layers. Large differences in the transcriptomes between stages and between the inner and the peripheral cells were found. SE attributes were expressed at the alveolus-cell-layer stage but were preferentially activated in the inner cell layers that resulted from periclinal division of the alveolus cell layer. Similarly, AL attributes started to be expressed only after the 2 L stage and were localized to the outermost peripheral cell layer. These results indicate that the first periclinal division of the alveolus cell layer is asymmetric at the transcriptome level, and that the cell-fate-specifying positional cues and their perception system are already operating before the first periclinal division. Several genes related to epidermal identity (i.e., type IV homeodomain-leucine zipper genes and wax biosynthetic genes) were also found to be expressed at the syncytial stage, but their expression was localized to the outermost peripheral cell layer from the 2 L stage onward. We believe that our findings significantly enhance our knowledge of the mechanisms underlying cell fate specification in rice endosperm.
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References
Abe M, Takahashi T, Komeda Y (2001) Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. Plant J 26:487–494. https://doi.org/10.1046/j.1365-313X.2001.01047.x
Akiba T, Hibara KI, Kimura F et al (2014) Organ fusion and defective shoot development in oni3 mutants of rice. Plant Cell Physiol 55:42–51. https://doi.org/10.1093/pcp/pct154
Akihiro T, Mizuno K, Fujimura T (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant Cell Physiol 46:937–946. https://doi.org/10.1093/pcp/pci101
Bach L, Michaelson LV, Haslam R et al (2008) The very-long-chain hydroxy fatty acyl-CoA dehydratase PASTICCINO2 is essential and limiting for plant development. Proc Natl Acad Sci U S A 105:14727–14731. https://doi.org/10.1073/pnas.0805089105
Beaudoin F, Wu X, Li F et al (2009) Functional characterization of the Arabidopsis β-ketoacyl-coenzyme a reductase candidates of the fatty acid elongase. Plant Physiol 150:1174–1191. https://doi.org/10.1104/pp.109.137497
Becraft PW (2007) Aleurone cell development. In: Olsen OA (eds) Endosperm. Plant cell monographs, vol 8, Springer, Berlin, Heidelberg, pp 45–56. https://doi.org/10.1007/7089_2007_108
Becraft PW (2001) Cell fate specification in the cereal endosperm. Semin Cell Dev Biol 12:387–394. https://doi.org/10.1006/scdb.2001.0268
Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maitain aleurone cell fate in maize endosperm development. Development 127:4039–4048. https://doi.org/10.1007/978-1-4020-8854-4_27
Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Dev 129:5217–5225. https://doi.org/10.1242/dev.129.22.5217
Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273:1406–1409. https://doi.org/10.1126/science.273.5280.1406
Becraft PW, Yi G (2011) Regulation of aleurone development in cereal grains. J Exp Bot 62:1669–1675. https://doi.org/10.1093/jxb/erq372
Bosnes M, Weideman F, Olsen OA (1992) Endosperm differentiation in barley wild-type and sex mutants. Plant J 2:661–674. https://doi.org/10.1111/j.1365-313X.1992.tb00135.x
Brown RC, Lemmon BE, Olsen OA (1994) Endosperm development in barley: Microtubule involvement in the morphogenetic pathway. Plant Cell 6:1241–1252. https://doi.org/10.1105/tpc.6.9.1241
Brown RC, Lemmon BE (2007) The developmental biology of cereal endosperm. Plant Cell Monogr 8:1–20. https://doi.org/10.1007/7089_2007_106
Brown RC, Lemmon BE (2001) The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 215:35–49. https://doi.org/10.1007/BF01280302
Brown RC, Lemmon BE, Nguyen H, Olsen OA (1999) Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 12:32–42. https://doi.org/10.1007/s004970050169
Brown R, Lemmon B, Olsen O (1996a) Development of the endosperm in rice (Oryza sativa L.): cellularization. J Plant Res 36:301–313. https://doi.org/10.1007/BF02344477
Brown RC, Lemmon BE, Olsen OA (1996b) Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma 192:168–177. https://doi.org/10.1007/BF01273889
Chen J, Zeng B, Zhang M et al (2014) Dynamic transcriptome landscape of maize embryo and endosperm development. Plant Physiol 166:252–264. https://doi.org/10.1104/pp.114.240689
Collart MA (2016) The Ccr4-Not complex is a key regulator of eukaryotic gene expression. Wiley Interdiscip Rev RNA 7:438–454. https://doi.org/10.1002/wrna.1332
Drea S, Leader DJ, Arnold BC et al (2005) Systematic spatial analysis of gene expression during wheat caryopsis development. Plant Cell 17:2172–2185. https://doi.org/10.1105/tpc.105.034058
Fuse T, Sasaki T, Yano M (2001) Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnol 18:219–222
Gehring M, Satyaki PR (2017) Endosperm and imprinting, inextricably linked. Plant Physiol 173:143–154. https://doi.org/10.1104/pp.16.01353
Geisler-Lee J, Gallie DR (2005) Aleurone cell identity is suppressed following connation in maize kernels. Plant Physiol 139:204–212. https://doi.org/10.1104/pp.105.064295
Gontarek BC, Neelakandan AK, Wu H, Becraft PW (2016) NKD transcription factors are central regulators of maize endosperm development. Plant Cell 28:2916–2936. https://doi.org/10.1105/tpc.16.00609
Greene TW, Hannah LC (1998) Maize endosperm ADP-glucose pyrophosphorylase SHRUNKEN2 and BRITTLE2 subunit interactions. Plant Cell 10:1295–1306. https://doi.org/10.1105/tpc.10.8.1295
Gruis D, Guo H, Selinger D et al (2006) Surface position, not signaling from surrounding maternal tissues, specifies aleurone epidermal cell fate in maize. Plant Physiol 141:898–909. https://doi.org/10.1104/pp.106.080945
Hara T, Katoh H, Ogawa D et al (2015) Rice SNF2 family helicase ENL1 is essential for syncytial endosperm development. Plant J 81:1–12. https://doi.org/10.1111/tpj.12705
Hattori T, Terada T, Hamasuna S (1995) Regulation of the Osem gene by abscisic acid and the transcriptional activator VP1: analysis of cis-acting promoter elements required for regulation by abscisic acid and VP1. Plant J 7:913–925
Hattori T, Terada T, Hamasuna ST (1994) Sequence and functional analyses of the rice gene homologous to the maize Vp1. Plant Mol Biol 24:805–810. https://doi.org/10.1007/BF00029862
Hibara K, Obara M, Hayashida E et al (2009) The ADAXIALIZED LEAF1 gene functions in leaf and embryonic pattern formation in rice. Dev Biol 334:345–354. https://doi.org/10.1016/j.ydbio.2009.07.042
Hoshikawa K (1967a) Studies on the development of endosperm in rice: 1. Process of endosperm tissue formation. Japanese J Crop Sci 36:151–161. https://doi.org/10.1626/jcs.36.151
Hoshikawa K (1967b) Studies on the development of endosperm in rice: 4. Differentiation and development of the aleurone lyaer. Jap J Crop Sci 2:216–220
Iida H, Yoshida A, Takada S (2019) ATML1 activity is restricted to the outermost cells of the embryo through post-transcriptional repressions. Development. https://doi.org/10.1242/dev.169300
Ishikawa R, Ohnishi T, Kinoshita Y et al (2011) Rice interspecies hybrids show precocious or delayed developmental transitions in the endosperm without change to the rate of syncytial nuclear division. Plant J 65:798–806. https://doi.org/10.1111/j.1365-313X.2010.04466.x
Ishimaru T, Ida M, Hirose S et al (2015) Laser microdissection-based gene expression analysis in the aleurone layer and starchy endosperm of developing rice caryopses in the early storage phase. Rice 8:1–15. https://doi.org/10.1186/s12284-015-0057-2
Ishimaru T, Matsuda T, Ohsugi R, Yamagishi T (2003) Morphological development of rice caryopses located at the different positions in a panicle from early to middle stage of grain filling. Funct Plant Biol 30:1139–1149. https://doi.org/10.1071/FP03122
Ishimoto K, Sohonahra S, Kishi-Kaboshi M et al (2019) Specification of basal region identity after asymmetric zygotic division requires mitogen-activated protein kinase 6 in rice. Development. https://doi.org/10.1242/dev.176305
Ito M, Sentoku N, Nishimura A et al (2002) Position dependent expression of gl2-type homeobox gene, roc1: Significance for protoderm differentiation and radial pattern formation in early rice embryogenesis. Plant J 29:497–507. https://doi.org/10.1046/j.1365-313x.2002.01234.x
Ito M, Sentoku N, Nishimura A et al (2003) Roles of rice GL2-type homeobox genes in epidermis differentiation. Breed Sci 53:245–253. https://doi.org/10.1270/jsbbs.53.245
Ito Y, Kimura F, Hirakata K et al (2011) Fatty acid elongase is required for shoot development in rice. Plant J 66:680–688. https://doi.org/10.1111/j.1365-313X.2011.04530.x
Javelle M, Vernoud V, Rogowsky PM, Ingram GC (2011) Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:17–39. https://doi.org/10.1111/j.1469-8137.2010.03514.x
Jeon JS, Ryoo N, Hahn TR et al (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 48:383–392. https://doi.org/10.1016/j.plaphy.2010.03.006
Jin P, Guo T, Becraft PW (2000) The maize CR4 receptor-like kinase mediates a growth factor-like differentiation response. Genesis 27:104–116.
Kessler S, Seiki S, Sinha N (2002) Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position. Development 129:1859–1869
Kiesselbach T (2001) The structure and reproduction of corn. Biol Plant 44:238–238. https://doi.org/10.1023/a:1010248820060
Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119. https://doi.org/10.1007/BF00279537
Kurdyukov S, Faust A, Trenkamp S et al (2006) Genetic and biochemical evidence for involvement of HOTHEAD in the biosynthesis of long-chain α-,ω-dicarboxylic fatty acids and formation of extracellular matrix. Planta 224:315–329. https://doi.org/10.1007/s00425-005-0215-7
Kuwano M, Masumura T, Yoshida KT (2011) A novel endosperm transfer cell-containing region-specific gene and its promoter in rice. Plant Mol Biol 76:47–56. https://doi.org/10.1007/s11103-011-9765-1
Larkin JC, Brown ML, Schiefelbein J (2003) How do cells know what they want to be when they grow up? Lessons from epidermal patterning in arabidopsis. Annu Rev Plant Biol 54:403–430. https://doi.org/10.1146/annurev.arplant.54.031902.134823
Lee SK, Hwang SK, Han M et al (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546. https://doi.org/10.1007/s11103-007-9153-z
Leroux BM, Goodyke AJ, Schumacher KI et al (2014) Maize early endosperm growth and development: Rom fertilization through cell type. Am J Bot 101:1259–1274. https://doi.org/10.3732/ajb.1400083
Lewis D, Bacic A, Chandler PM, Newbigin EJ (2009) Aberrant cell expansion in the elongation mutants of barley. Plant Cell Physiol 50:554–571. https://doi.org/10.1093/pcp/pcp015
Li M, Lopato S, Kovalchuk N, Langridge P (2013) Functional genomics of seed development in cereals. In: Gupta P, Varshney R (eds) Cereal Genomics II. Springer Netherlands, Dordrecht. https://doi.org/10.1007/978-94-007-6401-9_9
Lid SE, Al RH, Krekling T et al (2004) The maize disorganized aleurone layer 1 and 2 [dil1, dil2] mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm. Planta 218:370–378. https://doi.org/10.1007/s00425-003-1116-2
Lid SE, Gruis D, Jung R et al (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc Natl Acad Sci 99:5460–5465. https://doi.org/10.1073/pnas.042098799
Liu J, Wu X, Yao X et al (2018) Mutations in the DNA demethylase OsROS1 result in a thickened aleurone and improved nutritional value in rice grains. Proc Natl Acad Sci U S A 115:11327–11332. https://doi.org/10.1073/pnas.1806304115
Mi H, Ebert D, Muruganujan A et al (2020) PANTHER version 16: a revised family classification, tree-based classification tool, enhancer regions and extensive. Nucleic Acids Res. https://doi.org/10.1093/nar/gkaa1106
Miyoshi K, Kagaya Y, Ogawa Y et al (2002) Temporal and spatial expression pattern of the OSVP1 and OSEM genes during seed development in rice. Plant Cell Physiol 43:307–313. https://doi.org/10.1093/pcp/pcf040
Morrison IN, Kuo J, O’Brien TP (1975) Histochemistry and fine structure of developing wheat aleurone cells. Planta 123:105–116. https://doi.org/10.1007/BF00383859
Nakagawa T, Kurose T, Hino T et al (2007a) Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. J Biosci Bioeng 104:34–41. https://doi.org/10.1263/jbb.104.34
Nakagawa T, Suzuki T, Murata S et al (2007b) Improved gateway binary vectors: High-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci Biotechnol Biochem 71:2095–2100. https://doi.org/10.1271/bbb.70216
Nie DM, Ouyang YD, Wang X et al (2013) Genome-wide analysis of endosperm-specific genes in rice. Gene 530:236–247. https://doi.org/10.1016/j.gene.2013.07.088
Nishimura A, Aichi I, Matsuoka M (2007) A protocol for Agrobacterium-mediated transformation in rice. Nat Protoc 1:2796–2802. https://doi.org/10.1038/nprot.2006.469
Olsen O-A, Brown RC, Lemmon BE (1995) Pattern and process of wall formation in developing endosperm. BioEssays 17:803–812. https://doi.org/10.1002/bies.950170910
Olsen OA (2001) Endosperm development: Cellularization and cell fate specification. Annu Rev Plant Biol 52:233–267. https://doi.org/10.1146/annurev.arplant.52.1.233
Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:214–228. https://doi.org/10.1105/tpc.017111
Olsen OA (2020) The Modular Control of Cereal Endosperm Development. Trends Plant Sci 25:279–290. https://doi.org/10.1016/j.tplants.2019.12.003
Qing L, Aoyama T (2012) Pathways for epidermal cell differentiation via the homeobox gene GLABRA2: update on the roles of the classic egulator. J Integr Plant Biol 54:729–737. https://doi.org/10.1111/j.1744-7909.2012.01159.x
Qu J, Ma C, Feng J et al (2016) Transcriptome dynamics during maize endosperm development. PLoS One 11:1–22. https://doi.org/10.1371/journal.pone.0163814
Royo J, Gómez E, Hueros G (2007) Transfer Cells. In: Olsen OA (ed) Endosperm. Springer Berlin Heidelberg, Berlin, pp 73–89. https://doi.org/10.1007/7089_2007_110
Sato Y, Takehisa H, Kamatsuki K et al (2013) RiceXPro Version 3.0: Expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:1206–1213. https://doi.org/10.1093/nar/gks1125
Shen B, Li C, Min Z et al (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Natl Acad Sci U S A 100:6552–6557. https://doi.org/10.1073/pnas.0732023100
Suzuki K, Miyake H, Taniguchi T, Maeda E (2000) Cellularization of the free nuclear endosperm in rice caryopsis revealed by light and electron microscopy. Plant Prod Sci 3:446–458. https://doi.org/10.1626/pps.3.446
Takada S, Takada N, Yoshida A (2013) ATML1 promotes epidermal cell differentiation in Arabidopsis shoots. Development 140:1919–1923. https://doi.org/10.1242/dev.094417
Tanaka H, Watanabe M, Sasabe M et al (2007) Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134:1643–1652. https://doi.org/10.1242/dev.003533
Ueda M, Zhang Z, Laux T (2011) Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 Links zygote polarity to embryo development. Dev Cell 20:264–270. https://doi.org/10.1016/j.devcel.2011.01.009
Wisniewski JP, Rogowsky PM (2004) Vacuolar H+-translocating inorganic pyrophosphatase (Vpp1) marks partial aleurone cell fate in cereal endosperm development. Plant Mol Biol 56:325–337. https://doi.org/10.1007/s11103-004-3414-x
Wu H, Gontarek BC, Yi G et al (2020) The thick aleurone1 gene encodes a NOT1 subunit of the CCR4-NOT complex and regulates cell patterning in endosperm. Plant Physiol 184:960–972. https://doi.org/10.1104/pp.20.00703
Wu X, Liu J, Li D, Liu CM (2016) Rice caryopsis development II: Dynamic changes in the endosperm. J Integr Plant Biol 58:786–798. https://doi.org/10.1111/jipb.12488
Xu JJ, Zhang XF, Xue HW (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. J Exp Bot 67:6399–6411. https://doi.org/10.1093/jxb/erw409
Yephremov A, Wisman E, Huijser P et al (1999) Characterization of the FIDDLEHEAD gene of Arabidopsis reveals a link between adhesion response and cell differentiation in the epidermis. Plant Cell 11:2187–2201. https://doi.org/10.1105/tpc.11.11.2187
Yi G, Lauter AM, Paul Scott M, Becraft PW (2011) The thick aleurone1 mutant defines a negative regulation of maize aleurone cell fate that functions downstream of defective kernel. Plant Physiol 156:1826–1836. https://doi.org/10.1104/pp.111.177725
Yi G, Neelakandan AK, Gontarek BC et al (2015) The naked endosperm genes encode duplicate INDETERMINATE domain transcription factors required for maize endosperm cell patterning and differentiation. Plant Physiol 167:443–456. https://doi.org/10.1104/pp.114.251413
Zhan J, Thakare D, Ma C et al (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. https://doi.org/10.1105/tpc.114.135657
Acknowledgements
We thank Drs. M. Ueda and T. Nakagawa for their gifts of the plasmid carrying 3x(NLS-Venus) (MU110) and the plasmids used for the preparation of the Gateway-based vectors (pGW2Δ35S and pGWB500), respectively. This work was supported by JSPS KAKENHI (19K05968, 17H06471, and 20H00424) and by the National Institute of Genetics (NIG)-JOINT (54A2018, 12A2019, and 41A2020).
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Takafuji, Y., Shimizu-Sato, S., Ta, K.N. et al. High-resolution spatiotemporal transcriptome analyses during cellularization of rice endosperm unveil the earliest gene regulation critical for aleurone and starchy endosperm cell fate specification. J Plant Res 134, 1061–1081 (2021). https://doi.org/10.1007/s10265-021-01329-w
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DOI: https://doi.org/10.1007/s10265-021-01329-w