Molecular identification and functional verification of SPL9 and SPL15 of Lilium.


Journal

Molecular genetics and genomics : MGG
ISSN: 1617-4623
Titre abrégé: Mol Genet Genomics
Pays: Germany
ID NLM: 101093320

Informations de publication

Date de publication:
Jan 2022
Historique:
received: 09 03 2021
accepted: 30 10 2021
pubmed: 16 11 2021
medline: 8 2 2022
entrez: 15 11 2021
Statut: ppublish

Résumé

The transformation of plants from juveniles to adults is a key process in plant growth and development, and the main regulatory factors are miR156 and SQUAMOSA promoter binding protein-like (SPL) transcription factors. Lilium is an ornamental bulb, but it has a long maturation time. In this experiment, Lilium bulbs were subjected to a temperature treatment of 15 °C for 4 weeks to initiate vegetative phase change. Transmission electron microscopy indicated the cell wall of bud core tissue undergoing vegetative phase change became thinner, the starch grains were reduced, and the growth of the juvenile stage was accelerated. The key transcription factors LbrSPL9 and LbrSPL15 were cloned, and the phylogenetic analysis showed they possessed high homology with other plant SPLs. Subcellular localization and transcription activation experiments confirmed LbrSPL9 and LbrSPL15 were mainly located in the nucleus and exhibited transcriptional activity. The results of in situ hybridization showed the expression levels of LbrSPL9 and LbrSPL15 were increased after temperature change treatment. The functional verification experiment of the transgenic plants confirmed that the overexpression of LbrSPL9 and LbrSPL15 could shorten maturation time. These findings help elucidate the regulatory mechanisms of phase transition in Lilium and provide a reference for breeding research in other bulbous flowers.

Identifiants

pubmed: 34779936
doi: 10.1007/s00438-021-01832-8
pii: 10.1007/s00438-021-01832-8
doi:

Substances chimiques

Plant Proteins 0
Transcription Factors 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

63-74

Subventions

Organisme : Beijing Natural Science Fund-Municipal Education Commission
ID : KZ201810020029

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.

Références

Aguilar-Jaramillo AE, Marín-González E, Matias-Hernandez L, Osnato M, Suárez-López P (2019) TEMPRANILLO is a direct repressor of the microRNA miR172. Plant J 100(3):522–535
pubmed: 31310397
Cai C, Guo W, Zhang B (2018) Genome-wide identification and characterization of SPL transcription factor family and their evolution and expression profiling analysis in cotton. Sci Rep 8(1):49–63
Chen X, Zhang Z, Liu D, Zhang K, Li A, Mao L (2010) SQUAMOSA promoter-binding protein-like transcription factors: star players for plant growth and development. Integr Plant Biol 52:946–951
Chen LG, Gao Z, Zhao Z, Liu X, Tang W (2019) BZR1 family transcription factors function redundantly and indispensably in BR signaling but exhibit BRI1-independent function in regulating anther development in Arabidopsis. Mol Plant 12(10):1408–1415
pubmed: 31229643
Fan ZQ, Ba LJ, Shan W, Xiao YY, Lu WJ (2018) A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6. Plant 96:1191–1205
Gou J, Fu C, Liu S, Tang C, Debnath S, Flanagan A, Ge Y, Tang Y, Jiang Q, Larson PR, Wen J, Wang ZY (2017) The miR156-SPL4 module predominantly regulates aerial axillary bud formation and controls shoot architecture. New Phytol 216(3):829–840
pubmed: 28877340
Huang B, Qian P, Gao N, Shen J, Hou S (2017) Fackel interacts with gibberellic acid signaling and vernalization to mediate flowering in Arabidopsis. Planta 245(5):939–950
pubmed: 28108812
Hyun Y, Richter R, Vincent C, Rafael MG, Porri A, Coupland G (2016) Multi-layered regulation of SPL15 and cooperation with SOC1 integrate endogenous flowering pathways at the Arabidopsis shoot meristem. Dev Cell 37(3):254–266
pubmed: 27134142
Jayeni HB, Hayward A, O’Brien C, Ahsan U, Mitter N (2020) Phase change related microRNA profiles in the plant regeneration process of avocado through shoot-tip. Culture. https://doi.org/10.22606/as.2020.42001
doi: 10.22606/as.2020.42001
Jefferson RA, Kavangh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6(13):3901–3907
pubmed: 3327686 pmcid: 553867
Jia H, Xu ML, Willmann MR, McCormick K, Hu T, Yang L, Starker CG, Voytas DF, Meyers BC, Poethig RS (2018) Threshold-dependent repression of SPL gene expression by miR156/miR157 controls vegetative phase change in Arabidopsis thaliana. Plos Genet 14(4):e1007337
Jiang Y, Peng J, Wang M, Su W, Gao Y (2019) The role of EjSPL3, EjSPL4, EjSPL5 and EjSPL9 in regulating flowering in loquat (Eriobotrya japonic a Lindl). Int J of Mol Ences 21(1):248
Jin J, Zhou R, Liu H, Zhong C, Xie J, Qin Y, Qin YH (2020) The complete chloroplast genome of Lilium brownii F.E.Brown var. viridulum Baker (Liliaceae). Mitochondrial DNA Part B 5(1):986–987
pubmed: 33366839 pmcid: 7748718
John MP, Thomas GJ (2014) Chemistry and biological activity of steroidal glycosides from the Lilium genus. Nat Prod Rep 32:454–477
Jorgensen SA, Preston JC (2014) Differential SPL gene expression patterns reveal candidate genes underlying flowering time and architectural differences in Mimulus and Arabidopsis. Mol Phylogenet Evol 73:129–139
pubmed: 24508602
Jung JH, Seo PJ, Kang SK, Park CM (2011) miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Mol Biol 76:35–45
pubmed: 21373962
Kim HJ, Cho AR, Song SJ, Kim YJ (2016) Seed germination in response to diurnal fluctuations of temperature and GA3 treatment in Lilium tsingtauense Gilg. Hortic Abstr 10:189
Klein J, Saedler H, Huijser P (1996) A new family of DNA binding proteins includes putative transcriptional regulators of the Antirrhinum majus floral meristem identity gene SQUAMOSA. Mol Gen Genet 250(1):7–16
pubmed: 8569690
Lei KJ, Lin YM, Ren J, Bai L, Miao YC, An GY, Song CP (2016) Deficient responses by MicroRNA156 and its targeted SQUAMOSA promoter binding protein-like 3 in Arabidopsis. Plant Cell Physiol 57(1):192–203
pubmed: 26647245
Leichty AR, Poethig RS (2019) Development and evolution of age-dependent defenses in ant-acacias. Proc Natl Acad Sci USA 116(31):15596–15601
pubmed: 31308222 pmcid: 6681755
Li XY, Lin EP, Huang H, Niu MY, Tong ZK, Zhang JH (2018) Molecular characterization of SQUAMOSA promoter binding protein-like (SPL) gene family in Betula luminifera. Front Plant Sci 9:608–625
pubmed: 29780401 pmcid: 5945835
Li RJ, Li LM, Liu XL, Kim JC, Lu S (2019a) Diurnal regulation of plant epidermal wax synthesis through antagonistic roles of the transcription factors SPL9 and DEWAX. Plant Cell 31(11):2711–2733
pubmed: 31484683 pmcid: 6881124
Li RJ, Li LM, Liu XL, Kim JC, Jenks MA, Lü S (2019b) Diurnal regulation of plant epidermal wax synthesis through antagonistic roles of the transcription factors SPL9 and DEWAX. Plant Cell 31(11):2711–2733
pubmed: 31484683 pmcid: 6881124
Liu JD, Wilson TE, Milbrandt J, Johnston M (1993) Identifying DNA-binding sites and analyzing DNA-binding domains using a yeast selection system. Methods 5(2):125–137
Liu N, Tu L, Wang L, Hu HY, Xu J, Zhang XL (2017) MicroRNA 157-targeted SPL genes regulate floral organ size and ovule production in cotton. BMC Plant Biol 17(1):7
pubmed: 28068913 pmcid: 5223427
Liu HK, Yu Y, Deng YQ, Li J, Zhou SD (2018) The chloroplast genome of Lilium henrici: genome structure and comparative analysis. Molecules 23(6):1276–1289
pmcid: 6100032
Long JM, Liu CY, Feng MQ, Liu Y, Wu XM, Guo WW (2018) miR156-SPLs module regulates somatic embryogenesis induction in Citrus Callus. J Exp Bot 69(12):2979–2993
pubmed: 29659948 pmcid: 5972587
Mao HD, Yu LJ, Li ZJ, Yan Y, Han R, Liu H, Ma M (2016) Genome-wide analysis of the SPL family transcription factors and their responses to abiotic stresses in maize. Plant Gene 6:1–12
Mingli X, Tieqiang H, Zhao JF, Park MY, Keith WE, Wu G, Li Y, Poethig RS (2016) Developmental functions of miR156-regulated SQUAMOSA promoter binding protein-like (SPL) genes in Arabidopsis thaliana. PLoS Genet 12(8):e1006263
Ning K, Chen S, Huang H, Jiang J, Yuan HM, Li HY (2017) Molecular characterization and expression analysis of the SPL gene family with BpSPL9 transgenic lines found to confer tolerance to abiotic stress in Betula platyphylla Suk. Plant Cell Tissue Organ Cult 130(3):469–481
Peng XJ, Wang Q, Zhao Y, Li XY, Ma Q (2019) Comparative genome analysis of the SPL gene family reveals novel evolutionary features in maize. Genet Mol Biol 42(2):380–394
pubmed: 31271590 pmcid: 6726161
Peter H, Markus S (2011) The control of developmental phase transitions in plants. Development 138(19):4117–4129
Poethig RS (2010) The past, present, and future of vegetative phase change. Plant Physiol 154(2):541–544
pubmed: 20921181 pmcid: 2949024
Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152
pubmed: 23962841 pmcid: 4101000
Preston JC, Hileman LC (2013) Functional evolution in the plant SQUAMOSA-promoter binding protein-like (SPL) gene family. Front Plant Sci 4:1–13
Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P (2008) The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Mol Biol 67:183–195
pubmed: 18278578 pmcid: 2295252
Tian X, Xie J, Yu J (2020) Physiological and transcriptomic responses of Lanzhou lily (Lilium davidii, var unicolor) to cold stress. PLoS ONE 15(1):e0227921
pubmed: 31971962 pmcid: 6977731
Tripathi RK, Goel R, Kumari S, Dahuja A (2017) Genomic organization, phylogenetic comparison, and expression profiles of the SPL family genes and their regulation in soybean. Dev Genes Evol 227(2):101–119
pubmed: 28133699
Wang JW (2014) Regulation of flowering time by the miR156-mediated age pathway. J Exp Bot 65(17):4723–4730
pubmed: 24958896
Wang JW, Park MY, Wang LJ, Koo YJ, Chen XY, Weigel D, Poethig RS (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7(2):e1002012
pubmed: 21383862 pmcid: 3044678
Wang S, Wu K, Yuan Q, Liu X, Liu Z, Lin X, Zeng R, Zhu H, Dong G, Qian Q (2012) Control of grain size, shape and quality by OsSPL16 in rice. Nat Genet 44(8):950–954
pubmed: 22729225
Wang Y, Wu F, Bai J, He Y (2013) BrpSPL9 (Brassica rapa ssp. pekinensis SPL9) controls the earliness of heading time in Chinese cabbage. Plant Biotechnol J 12(3):312–321
pubmed: 24237584
Wang BJ, Wang J, Wang C, Shen W, Jia H, Zhu X, Li X (2016) Study on expression modes and cleavage role of miR156b/c/d and its target gene Vv-SPL9 during the whole growth stage of Grapevine. J Hered 107(7):626–634
pubmed: 27660497
Wang Z, Zhu T, Ma W, Lu N, Wang J (2020) Potential function of CbuSPL and gene encoding its interacting protein during flowering in Catalpa bungei. BMC Plant Biol 20(2):40–51
Wei Q, Ma C, Xu YJ, Wang TL, Chen YY, Lü J, Zhang LL, Jiang CZ, Hong B, Gao JP (2017) Control of chrysanthemum flowering through integration with an aging pathway. Nat Commun 8(1):829
pubmed: 29018260 pmcid: 5635119
Wei HB, Zhao YP, Xie YR, Wang HY (2018) Exploiting SPL genes to improve maize plant architecture tailored for high-density planting. J Exp Bot 69(20):4675–4688
pubmed: 29992284
Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750–759
pubmed: 19703400 pmcid: 2732587
Yan Y, Wei MX, Li Y, Tao H, Wu H, Chen Z, Li C, Xu JH (2020) MiR529a controls plant height, tiller number, panicle architecture and grain size by regulating SPL target genes in rice (Oryza sativa L.). Plant Sci 302:110728
pubmed: 33288029
Yang L, Xu M, Koo Y, He JJ, Poethig RS (2013) Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. Elife 2(2):e00260
pubmed: 23538384 pmcid: 3608266
Yoshikawa T, Ozawa S, Sentoku N, Itoh JI, Yokoi S (2013) Change of shoot architecture during juvenile-to-adult phase transition in soybean. Planta 238(1):229–237
pubmed: 23686337
Yu ZX, Wang LJ, Zhao B, Shan CM, Zhang YH, Chen DF, Chen XY (2015) Progressive regulation of sesquiterpene biosynthesis in Arabidopsis and patchouli (Pogostemon cablin) by the miR156-targeted SPL transcription factors. Mol Plant 8(1):98–110
pubmed: 25578275
Yu N, Yang JC, Yin GT, Li RS, Zou WT (2020) Genome-wide characterization of the SPL gene family involved in the age development of Jatropha curcas. BMC Genomics 21(2):585–596
Zechmann B, Zellnig G (2010) Microwave-assisted rapid plant sample preparation for transmission electron microscopy. J Microsc 233(2):258–268
Zhang TQ, Wang JW, Zhou CM (2015) The role of miR156 in developmental transitions in Nicotiana tabacum. Sci China Life Sci 58(3):253–260
pubmed: 25682394
Zhang H, Zhang L, Han J, Qian B, Zhou Y (2019) The nuclear localization signal is required for the function of squamosa promoter binding protein-like gene 9 to promote vegetative phase change in Arabidopsis. Plant Mol Biol 100(6):571–578
pubmed: 30953277
Zhang D, Han Z, Li J, Qin H, Zhou L, Wang Y, Zhu X, Ma YC, Fang W (2020) Genome-wide analysis of the SBP-box gene family transcription factors and their responses to abiotic stresses in tea (Camellia sinensis). Genomics 112(3):2194–2202
pubmed: 31870711

Auteurs

Mengna Zhao (M)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.

Rongxiu Liu (R)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.

Yao Chen (Y)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.

Jinteng Cui (J)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China.
Beijing Laboratory of Urban and Rural Ecological Environment, Beijing, 102206, People's Republic of China.

Wei Ge (W)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China. 2562860102@qq.com.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China. 2562860102@qq.com.
Beijing Laboratory of Urban and Rural Ecological Environment, Beijing, 102206, People's Republic of China. 2562860102@qq.com.

Kezhong Zhang (K)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing University of Agriculture, Beijing, 102206, People's Republic of China. zhangkezhongbua@163.com.
College of Landscape Architecture, Beijing University of Agriculture, Beijing, 102206, People's Republic of China. zhangkezhongbua@163.com.
Beijing Laboratory of Urban and Rural Ecological Environment, Beijing, 102206, People's Republic of China. zhangkezhongbua@163.com.

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