Genome-wide evolutionary characterization and expression analysis of SIAMESE-RELATED family genes in maize
Tóm tắt
The SIAMESE (SIM) locus is a cell-cycle kinase inhibitor (CKI) gene that has to date been identified only in plants; it encodes a protein that promotes transformation from mitosis to endoreplication. Members of the SIAMESE-RELATED (SMR) family have similar functions, and some are related to cell-cycle responses and abiotic stresses. However, the functions of SMRs are poorly understood in maize (Zea mays L.). In the present study, 12 putative SMRs were identified throughout the entire genome of maize, and these were clustered into six groups together with the SMRs from seven other plant species. Members of the ZmSMR family were divided into four groups according to their protein sequences. Various cis-acting elements in the upstream sequences of ZmSMRs responded to abiotic stresses. Expression analyses revealed that all ZmSMRs were upregulated at 5, 20, 25, and 35 days after pollination. In addition, we found that ZmSMR9/11/12 may have regulated the initiation of endoreplication in endosperm central cells. Additionally, ZmSMR2/10 may have been primarily responsible for the endoreplication regulation of outer endosperm or aleurone cells. The relatively high expression levels of almost all ZmSMRs in the ears and tassels also implied that these genes may function in seed development. The effects of treatments with ABA, heat, cold, salt, and drought on maize seedlings and expression of ZmSMR genes suggested that ZmSMRs were strongly associated with response to abiotic stresses. The present study is the first to conduct a genome-wide analysis of members of the ZmSMR family by investigating their locations in chromosomes, identifying regulatory elements in their promoter regions, and examining motifs in their protein sequences. Expression analysis of different endosperm developmental periods, tissues, abiotic stresses, and hormonal treatments suggests that ZmSMR genes may function in endoreplication and regulate the development of reproductive organs. These results may provide valuable information for future studies of the functions of the SMR family in maize.
Tài liệu tham khảo
Dewitte W, Murray JA. The plant cell cycle. Annu Rev Plant Biol. 2003;54:235–64.
Ramirez-Parra E, Desvoyes B, Gutierrez C. Balance between cell division and differentiation during plant development. Int J Dev Biol. 2005;49(5–6):467–77.
Edgar BA, Orr-Weaver TL. Endoreplication cell cycles more for less. Cell. 2001;105:297–306.
Larkins BA, Dilkes BP, Dante RA, Coelho CM. Investigating the hows and whys of DNA endoreduplication. J Exp Bot. 2001;52(355):183–92.
D’Amato F. Role of polyploidy in reproductive organs and tissues. In: Johri BM, editor. Embryology of angiosperms. Berlin: Springer; 1984. p. 519–66.
Inze D, De Veylder L. Cell cycle regulation in plant development. Annu Rev Genet. 2006;40:77–105.
Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, Hofte H. Cellular basis of hypocotyl growth in Arabidopsis thaliana. Plant Physiol. 1997;114(1):295–305.
Kudo N, Kimura Y. Nuclear DNA endoreduplication during petal development in cabbage: relationship between ploidy levels and cell size. J Exp Bot. 2002;53(371):1017–23.
Kladnik A, Chourey PS, Pring DR, Dermastia M. Development of the endosperm of Sorghum bicolor during the endoreduplication-associated growth phase. J Cereal Sci. 2006;43(2):209–15.
Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, et al. Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiol. 2005;139(4):1984–94.
Jakoby M, Schnittger A. Cell cycle and differentiation. Curr Opin Plant Biol. 2004;7(6):661–9.
Melaragno JE, Mehrotra B, Coleman AW. Relationship between Endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell. 1993;5(11):1661–8.
Ceccarelli M, Santantonio E, Marmottini F, Amzallag GN, Cionini PG. Chromosome endoreduplication as a factor of salt adaptation in Sorghum bicolor. Protoplasma. 2006;227(2–4):113–8.
Engelen-Eigles G, Jones RJ, Phillips RL. DNA endoreduplication in maize endosperm cells: the effect of exposure to short-term high temperature. Plant Cell Environ. 2000;23(6):657–63.
Barow M. Endopolyploidy in seed plants. BioEssays. 2006;28(3):271–81.
Jin X, Fu Z, Lv P, Peng Q, Ding D, Li W, et al. Identification and characterization of microRNAs during maize grain filling. PLoS One. 2015;10(5):e0125800.
Sabelli PA, Leiva-Neto JT, Dante RA, Hong N, Larkins BA. Cell cycle regulation during maize endosperm development. Maydica. 2005;50:485–96.
Kowles RV, Phillips RL. Endosperm development in maize. Int Rev Cytol. 1988;112:97–136.
Sun Y, Flannigan BA, Setter TL. Regulation of endoreduplication in maize (Zea mays L.) endosperm. Isolation of a novel B1-type cyclin and its quantitative analysis. Plant Mol Biol. 1999;41(2):245–58.
Dante RA. Characterization of cyclin-dependent kinases and their expression in developing maize endosperm [electronic resource]. Tucson: The University of Arizona; 2005.
Sun Y, Dilkes BP, Zhang C, Dante RA, Carneiro NP, Lowe KS, et al. Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc Natl Acad Sci U S A. 1999;96(7):4180–5.
Coelho CM, Dante RA, Sabelli PA, Sun Y, Dilkes BP, Gordon-Kamm WJ, et al. Cyclin-dependent kinase inhibitors in maize endosperm and their potential role in endoreduplication. Plant Physiol. 2005;138(4):2323–36.
Sabelli PA, Dante RA, Leiva-Neto JT, Jung R, Gordon-Kamm WJ, Larkins BA. RBR3, a member of the retinoblastoma-related family from maize, is regulated by the RBR1/E2F pathway. Proc Natl Acad Sci U S A. 2005;102(37):13005–12.
Sabelli PA, Larkins BA. Grasses like mammals redundancy and compensatory regulation within the retinoblastoma protein family. Cell Cycle. 2006;5(4):352–5.
Kim JC, Laparra H, Calderon-Urrea A, Mottinger JP, Moreno MA, Dellaporta SL. Cell cycle arrest of stamen initials in maize sex determination. Genetics. 2007;177(4):2547–51.
Larkin JC, Brown ML, Schiefelbein J. How do cells know what they want to be when they grow up? Lessons from epidermal patterning in Arabidopsis. Annu Rev Plant Biol. 2003;54:403–30.
Bramsiepe J, Wester K, Weinl C, Roodbarkelari F, Kasili R, Larkin JC, et al. Endoreplication controls cell fate maintenance. PLoS Genet. 2010;6(6):e1000996.
Walker JD, Oppenheimer DG, Concienne J, Larkin JC. SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development. 2000;127(18):3931–40.
Churchman ML, Brown ML, Kato N, Kirik V, Hulskamp M, Inze D, et al. SIAMESE, a plant-specific cell cycle regulator, controls endoreplication onset in Arabidopsis thaliana. Plant Cell. 2006;18(11):3145–57.
Rogers S, Wells R, Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science (New York, NY). 1986;234(4774):364–8.
He J, Wang D, Zhang J, Wang Y. Functional analysis of the fruit-specific promoter of VqSTS6 from the Chinese wild grape, Vitis quinquangularis. Agri Gene. 2016;1:38–45.
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.
Frolov V. M: functional antagonism between E2F family members. Genes Dev. 2001;15(16):2146–60.
Zhang J, Zhang X, Wang Y, Hou H, Qian Y. Characterization of sequence elements from Malvastrum yellow vein betasatellite regulating promoter activity and DNA replication. Virol J. 2012;9(234):2–9.
Zhang ZY, Zhao J, Hu Y, Zhang TZ. Isolation of GhMYB9 gene promoter and characterization of its activity in transgenic cotton. Biologia Plantarum Vol. 2015;59(4):629–36.
Medina J, Bargues M, Terol J, Pe’rez-Alonso M, Salinas J. The Arabidopsis CBF gene family is composed of three genes encoding AP2 domain-containing proteins whose expression is regulated by low temperature but not by abscisic acid or dehydration. Plant Physiol. 1999;119(2):463–9.
Barcala M, García A, Cubas P, Almoguera C, Jordano J, Fenoll C, et al. Distinct heat-shock element arrangements that mediate the heat shock, but not the late-embryogenesis induction of small heat-shock proteins, correlate with promoter activation in root-knot nematode feeding cells. Plant Mol Biol. 2007;66(1–2):151–64.
Hobo T, Asada M, Kowyama Y, Hattori T. ACGT-containing abscisic acid response element (ABRE) and coupling element 3 (CE3) are functionally equivalent. Plant J. 1999;19(6):679–89.
Freeling M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol. 2009;60:433–53.
SanMiguel P, Gaut BS, Tikhonov A, Nakajima Y, Bennetzen JL. The paleontology of intergene retrotransposons of maize. Nat Genet. 1998;20(1):43–5.
Peres A, Churchman ML, Hariharan S, Himanen K, Verkest A, Vandepoele K, et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J Biol Chem. 2007;282(35):25588–96.
De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, et al. Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell. 2001;13(7):1653–68.
Kumar N, Harashima H, Kalve S, Bramsiepe J, Wang K, Sizani BL, et al. Functional conservation in the SIAMESE-RELATED family of cyclin-dependent kinase inhibitors in land plants. Plant Cell. 2015;27(11):3065–80.
Kay BK, Williamson MP, Sudol M. The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J. 2000;14(2):231–41.
Sabelli PA, Larkins BA. The contribution of cell cycle regulation to endosperm development. Sex Plant Reprod. 2009;22(4):207–19.
Cao J. Analysis of the Prefoldin gene family in 14 plant species. Front Plant Sci. 2016;7:317.
Singh AK, Sharma V, Pal AK, Acharya V, Ahuja PS. Genome-wide organization and expression profiling of the NAC transcription factor family in potato (Solanum tuberosum L.). DNA Res. 2013;20(4):403–23.
Yi D, Alvim Kamei CL, Cools T, Vanderauwera S, Takahashi N, Okushima Y, et al. The Arabidopsis SIAMESE-RELATED cyclin-dependent kinase inhibitors SMR5 and SMR7 regulate the DNA damage checkpoint in response to reactive oxygen species. Plant Cell. 2014;26(1):296–309.
Grafi G, Larkins BA. Endoreduplication in maize Endosperm_ involvement of M phase--promoting factor inhibition and induction of S phase--related kinases. Science. 1995;269(5228):1262–4.
Nemhauser JL, Hong F, Chory J. Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell. 2006;126(3):467–75.
Setter TL, Flannigan BA. Water deficit inhibits cell division and expression of transcripts involved in cell proliferation and endoreduplication in maize endosperm. J Exp Bot. 2001;52(360):1401–8.
Artlip TS, Madison JT, Setter TL. Water deficit in developing endosperm of maize_ cell division and nuclear DNA endoreduplication. Plant Cell Environ. 1995;18(9):1034–40.
Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, et al. Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot. 2014;65(22):6629–44.
Zhao P, Wang D, Wang R, Kong N, Zhang C, Yang C, et al. Genome-wide analysis of the potato Hsp20 gene family: identification, genomic organization and expression profiles in response to heat stress. BMC Genomics. 2018;19(1):61.
Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY, et al. PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res. 2016;44(D1):D1154–60.
Solovyev VV, Shahmuradov IA, Salamov AA. Identification of promoter regions and regulatory sites. Methods Mol Biol. 2010;674:57–83.
Shahmuradov IA, Solovyev VV. Nsite, NsiteH and NsiteM computer tools for studying transcription regulatory elements. Bioinformatics. 2015;31(21):3544–5.
Lyons E, Pedersen B, Kane J, Freeling M. The value of nonmodel genomes and an example using SynMap within CoGe to dissect the Hexaploidy that predates the Rosids. Trop Plant Biol. 2008;1(3–4):181–90.
Miao Z, Han Z, Zhang T, Chen S, Ma C. A systems approach to a spatio-temporal understanding of the drought stress response in maize. Sci Rep. 2017;7(1):6590.
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28(10):2731–9.
Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34:W369–73 Web Server issue.
Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 2009;37:W202–8 Web Server issue.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 2001;25(4):402–8.