Functional homoeologous alleles of CONSTANS contribute to seasonal crop type in rapeseed.

Szczegóły
Abstrakt

Tytuł:: Functional homoeologous alleles of CONSTANS contribute to seasonal crop type in rapeseed.
Autorzy:: Jin Q; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Yin S; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Li G; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Guo T; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Wan M; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Li H; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.; School of Life Sciences, Hubei University, Wuhan, 430062, China.
Li J; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Ge X; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
King GJ; Southern Cross Plant Science, Southern Cross University, Lismore, NSW, 2480, Australia.
Li Z; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Wang J; National Key Lab of Crop Genetic Improvement, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China. .
Zhou G; College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
Źródło:: TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik [Theor Appl Genet] 2021 Oct; Vol. 134 (10), pp. 3287-3303. Date of Electronic Publication: 2021 Aug 19.
Typ publikacji:: Journal Article
Język:: English
Imprint Name(s):: Original Publication: Berlin, New York, Springer
MeSH Terms:: Gene Expression Regulation, Plant*
Phenotype*
Brassica napus/*growth & development
Chromosomes, Plant/*genetics
Flowers/*growth & development
Plant Proteins/*metabolism
Transcription Factors/*metabolism
Alleles ; Brassica napus/genetics ; Chromosome Mapping/methods ; Ecotype ; Evolution, Molecular ; Flowers/genetics ; Photoperiod ; Phylogeny ; Plant Breeding ; Plant Proteins/genetics ; Quantitative Trait Loci ; Seasons ; Transcription Factors/genetics
References:: Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, Coupland G, Samach A, Lifschitz E (2006) The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J 46(3):462–476. https://doi.org/10.1111/j.1365-313X.2006.02706.x. (PMID: 10.1111/j.1365-313X.2006.02706.x16623906)
Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH (2010) The role of recently derived ft para logs in sunflower domestication. Curr Biol 20(7):629–635. https://doi.org/10.1016/j.cub.2010.01.059. (PMID: 10.1016/j.cub.2010.01.059203032652898918)
Campoli C, Drosse B, Searle I, Coupland G, von Korff M (2012) Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J 69:868–880. https://doi.org/10.1111/j.1365-313X.2011.04839.x. (PMID: 10.1111/j.1365-313X.2011.04839.x22040323)
Chalhoub B et al (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345(6199):950–953. https://doi.org/10.1126/science.1253435. (PMID: 10.1126/science.1253435)
Chen L, Dong F, Cai J, Xin Q, Fang C, Liu L, Wan L, Yang G, Hong D (2018) A 2.833-kb insertion in BnFLC.A2 and its homeologous exchange with BnFLC.C2 during breeding selection generated early-flowering rapeseed. Mol Plant 11(1):222–225. https://doi.org/10.1016/j.molp.2017.09.020. (PMID: 10.1016/j.molp.2017.09.02029024744)
Cheng F, Mandakova T, Wu J, Xie Q, Lysak MA, Wang X (2013) Deciphering the diploid ancestral genome of the mesohexaploid Brassica rapa. Plant Cell 25(5):1541–1554. https://doi.org/10.1105/tpc.113.110486. (PMID: 10.1105/tpc.113.110486236534723694691)
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x. (PMID: 10.1046/j.1365-313x.1998.00343.x)
Gonzalez-Schain ND, Diaz-Mendoza M, Zurczak M, Suarez-Lopez P (2012) Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J 70(4):678–690. https://doi.org/10.1111/j.1365-313X.2012.04909.x. (PMID: 10.1111/j.1365-313X.2012.04909.x22260207)
Gookin TE, Assmann SM (2014) Significant reduction of BiFC non-specific assembly facilitates in planta assessment of heterotrimeric G-protein interactors. Plant J 80(3):553–567. https://doi.org/10.1111/tpj.12639. (PMID: 10.1111/tpj.12639251870414260091)
Griffiths S, Dunford RP, Coupland G, Laurie DA (2003) The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol 131(4):1855–1867. https://doi.org/10.1104/pp.102.016188. (PMID: 10.1104/pp.102.01618812692345166942)
Haudry A et al (2013) An atlas of over 90,000 conserved noncoding sequences provides insight into crucifer regulatory regions. Nat Genet 45(8):891-U228. https://doi.org/10.1038/ng.2684. (PMID: 10.1038/ng.268423817568)
Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K (2003) Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422(6933):719–722. https://doi.org/10.1038/nature01549. (PMID: 10.1038/nature0154912700762)
Helliwell CA, Wood CC, Robertson M, Peacock WJ, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46(2):183–192. https://doi.org/10.1111/j.1365-313X.2006.02686.x. (PMID: 10.1111/j.1365-313X.2006.02686.x16623882)
Hou J, Long Y, Raman H, Zou X, Wang J, Dai S, Xiao Q, Li C, Fan L, Liu B, Meng J (2012) A Tourist-like MITE insertion in the upstream region of the BnFLC. A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L.). BMC plant biology. https://doi.org/10.1186/1471-2229-12-238. (PMID: 10.1186/1471-2229-12-238232412443562271)
Jiao Y, Wickett NJ, Ayyampalayam S, Chanderbali AS, Landherr L, Ralph PE, Tomsho LP, Hu Y, Liang H, Soltis PS, Soltis DE, Clifton SW, Schlarbaum SE, Schuster SC, Ma H, Leebens-Mack J, dePamphilis CW (2011) Ancestral polyploidy in seed plants and angiosperms. Nature 473(7345):97-U113. https://doi.org/10.1038/nature09916. (PMID: 10.1038/nature0991621478875)
Lagercrantz U, Axelsson T (2000) Rapid evolution of the family of CONSTANS LIKE genes in plants. Mol Biol Evol 17(10):1499–1507. https://doi.org/10.1093/oxfordjournals.molbev.a026249. (PMID: 10.1093/oxfordjournals.molbev.a02624911018156)
Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and clustal X version 2.0. Bioinformatics 23(21):2947–2948. (PMID: 10.1093/bioinformatics/btm404)
Liu S et al (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun. https://doi.org/10.1038/ncomms4930. (PMID: 10.1038/ncomms4930255245304321900)
Long Y, Shi J, Qiu D, Li R, Zhang C, Wang J, Hou J, Zhao J, Shi L, Park B-S, Choi SR, Lim YP, Meng J (2007) Flowering time quantitative trait loci analysis of oilseed Brassica in multiple environments and genomewide alignment with Arabidopsis. Genetics 177(4):2433–2444. https://doi.org/10.1534/genetics.107.080705. (PMID: 10.1534/genetics.107.080705180734392219480)
Lysak MA, Koch MA, Pecinka A, Schubert I (2005) Chromosome triplication found across the tribe Brassiceae. Genome Res 15(4):516–525. https://doi.org/10.1101/gr.3531105. (PMID: 10.1101/gr.3531105157815731074366)
Lysak MA, Berr A, Pecinka A, Schmidt R, McBreen K, Schubert I (2006) Mechanisms of chromosome number reduction in Arabidopsis thaliana and related Brassicaceae species. Proc Natl Acad Sci USA 103(13):5224–5229. https://doi.org/10.1073/pnas.0510791103. (PMID: 10.1073/pnas.0510791103165497851458822)
Nagaharu U (1935) Genomic analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. J Japanese Bot 7:389–452.
Perumal S, Koh CS, Jin L, Buchwaldt M, Higgins EE, Zheng C, Sankoff D, Robinson SJ, Kagale S, Navabi Z-K, Tang L, Horner KN, He Z, Bancroft I, Chalhoub B, Sharpe AG, Parkin IAP (2020) A high-contiguity Brassica nigra genome localizes active centromeres and defines the ancestral Brassica genome. Nat Plants. https://doi.org/10.1038/s41477-020-0735-y. (PMID: 10.1038/s41477-020-0735-y327824087419231)
Putterill J, Robson F, Lee K, Simon R, Coupland G (1995) The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc-finger transcription factors. Cell 80(6):847–857. https://doi.org/10.1016/0092-8674(95)90288-0. (PMID: 10.1016/0092-8674(95)90288-07697715)
Quijada PA, Udall JA, Lambert B, Osborn TC (2006) Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed Brassica napus L Identification of genomic regions from winter germplasm. Theor Appl Gene 113(3):549–561. (PMID: 10.1007/s00122-006-0323-1)
Raman H, Raman R, Coombes N, Song J, Prangnell R, Bandaranayake C, Tahira R, Sundaramoorthi V, Killian A, Meng J, Dennis ES, Balasubramanian S (2016) Genome-wide association analyses reveal complex genetic architecture underlying natural variation for flowering time in canola. Plant Cell Environ 39(6):1228–1239. https://doi.org/10.1111/pce.12644. (PMID: 10.1111/pce.1264426428711)
Raman H, Raman R, Qiu Y, Yadav AS, Sureshkumar S, Borg L, Rohan M, Wheeler D, Owen O, Menz I, Balasubramanian S (2019) GWAS hints at pleiotropic roles for FLOWERING LOCUS T in flowering time and yield-related traits in canola. BMC Genomics. https://doi.org/10.1186/s12864-019-5964-y. (PMID: 10.1186/s12864-019-5964-y313875216685183)
Robert LS, Robson F, Sharpe A, Lydiate D, Coupland G (1998) Conserved structure and function of the Arabidopsis flowering time gene CONSTANS in Brassica napus. Plant Mol Biol 37(5):763–772. https://doi.org/10.1023/a:1006064514311. (PMID: 10.1023/a:10060645143119678571)
Robson F, Costa MMR, Hepworth SR, Vizir I, Pineiro M, Reeves PH, Putterill J, Coupland G (2001) Functional importance of conserved domains in the flowering-time gene CONSTANS demonstrated by analysis of mutant alleles and transgenic plants. Plant J 28(6):619–631. https://doi.org/10.1046/j.1365-313x.2001.01163.x. (PMID: 10.1046/j.1365-313x.2001.01163.x11851908)
Rosas U, Mei Y, Xie Q, Banta JA, Zhou RW, Seufferheld G, Gerard S, Chou L, Bhambhra N, Parks JD, Flowers JM, McClung CR, Hanzawa Y, Purugganan MD (2014) Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS. Nat Commun. https://doi.org/10.1038/ncomms4651. (PMID: 10.1038/ncomms465124736505)
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288(5471):1613–1616. https://doi.org/10.1126/science.288.5471.1613. (PMID: 10.1126/science.288.5471.161310834834)
Schiessl S (2020) Regulation and subfunctionalization of flowering time genes in the allotetraploid oil crop Brassica napus. Front Plant Sci. https://doi.org/10.3389/fpls.2020.605155. (PMID: 10.3389/fpls.2020.605155333296787718018)
Schiessl S, Samans B, Huettel B, Reinhard R, Snowdon RJ (2014) Capturing sequence variation among flowering-time regulatory gene homologs in the allopolyploid crop species Brassica napus. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00404. (PMID: 10.3389/fpls.2014.00404252023144142343)
Searle I, He YH, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20(7):898–912. https://doi.org/10.1101/gad.373506. (PMID: 10.1101/gad.373506166009151472290)
Shi L, Song J, Guo C, Wang B, Guan Z, Yang P, Chen X, Zhang Q, King GJ, Wang J, Liu K (2019) A CACTA-like transposable element in the upstream region of BnaA9 CYP78A9 acts as an enhancer to increase silique length and seed weight in rapeseed. Plant Journal 98(3):524–539. (PMID: 10.1111/tpj.14236)
Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138(2):1163–1173. https://doi.org/10.1104/pp.105.061309. (PMID: 10.1104/pp.105.061309159085961150429)
Simon S, Ruehl M, de Montaigu A, Woetzel S, Coupland G (2015) Evolution of CONSTANS regulation and function after gene duplication produced a photoperiodic flowering switch in the brassicaceae. Mol Biol Evol 32(9):2284–2301. https://doi.org/10.1093/molbev/msv110. (PMID: 10.1093/molbev/msv110259723464540966)
Simpson GG, Dean C (2002) Flowering - Arabidopsis, the rosetta stone of flowering time? Science 296(5566):285–289. https://doi.org/10.1126/science.296.5566.285. (PMID: 10.1126/science.296.5566.28511951029)
Song YH, Lee I, Lee SY, Imaizumi T, Hong JC (2012) CONSTANS and ASYMMETRIC LEAVES 1 complex is involved in the induction of FLOWERING LOCUS T in photoperiodic flowering in Arabidopsis. Plant J 69(2):332–342. https://doi.org/10.1111/j.1365-313X.2011.04793.x. (PMID: 10.1111/j.1365-313X.2011.04793.x21950734)
Song JM, Guan Z, Hu J, Guo C, Yang Z, Wang S, Liu D, Wang B, Lu S, Zhou R, Xie WZ, Cheng Y, Zhang Y, Liu K, Yang QY, Chen LL, Guo L (2020) Eight high-quality genomes reveal pan-genome architecture and ecotype differentiation of Brassica napus. Nature Plants 6(1):34–45. https://doi.org/10.1038/s41477-019-0577-7. (PMID: 10.1038/s41477-019-0577-7319326766965005)
Takahashi Y, Shimamoto K (2011) Heading date 1 (Hd1), an ortholog of Arabidopsis CONSTANS, is a possible target of human selection during domestication to diversify flowering times of cultivated rice. Genes Genet Syst 86(3):175–182. (PMID: 10.1266/ggs.86.175)
Tiwari SB, Shen Y, Chang H-C, Hou Y, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C, Belachew A, Repetti PP, Reuber TL, Ratcliffe OJ (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187(1):57–66. https://doi.org/10.1111/j.1469-8137.2010.03251.x. (PMID: 10.1111/j.1469-8137.2010.03251.x20406410)
Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594. https://doi.org/10.1146/annurev.arplant.59.032607.092755. (PMID: 10.1146/annurev.arplant.59.032607.09275518444908)
Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949–956. https://doi.org/10.1046/j.1365-313X.2003.01676.x. (PMID: 10.1046/j.1365-313X.2003.01676.x12609035)
Wang X et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035-U1157. https://doi.org/10.1038/ng.919. (PMID: 10.1038/ng.91921873998)
Wei FJ, Tsai YC, Wu HP, Huang LT, Chen YC, Chen YF, Wu CC, Tseng YT, YiC H (2016) Both Hd1 and Ehd1 are important for artificial selection of flowering time in cultivated rice. Plant Sci 242:187–194. https://doi.org/10.1016/j.plantsci.2015.09.005. (PMID: 10.1016/j.plantsci.2015.09.00526566836)
Wu D, Liang Z, Yan T, Xu Y, Xuan L, Tang J, Zhou G, Lohwasser U, Hua S, Wang H, Chen X, Wang Q, Zhu L, Maodzeka A, Hussain N, Li Z, Li X, Shamsi IH, Jilani G, Wu L, Zheng H, Zhang G, Chalhoub B, Shen L, Yu H, Jiang L (2019) Whole-genome resequencing of a worldwide collection of rapeseed accessions reveals the genetic basis of ecotype divergence. Mol Plant 12(1):30–43. https://doi.org/10.1016/j.molp.2018.11.007. (PMID: 10.1016/j.molp.2018.11.00730472326)
Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40(6):761–767. https://doi.org/10.1038/ng.143. (PMID: 10.1038/ng.14318454147)
Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100(10):6263–6268. https://doi.org/10.1073/pnas.0937399100. (PMID: 10.1073/pnas.093739910012730378156360)
Yang J, Liu D, Wang X, Ji C, Cheng F, Liu B, Hu Z, Chen S, Pental D, Ju Y, Yao P, Li X, Xie K, Zhang J, Wang J, Liu F, Ma W, Shopan J, Zheng H, Mackenzie SA, Zhang M (2016) The genome sequence of allopolyploid Brassica juncea and analysis of differential homoeolog gene expression influencing selection. Nat Genet 48(10):1225–1232. https://doi.org/10.1038/ng.3657. (PMID: 10.1038/ng.365727595476)
Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the arabidopsis flowering time gene CONSTANS. Plant Cell 12(12):2473–2483. https://doi.org/10.1105/tpc.12.12.2473. (PMID: 10.1105/tpc.12.12.247311148291102231)
Yi L, Chen C, Yin S, Li H, Li Z, Wang B, King GJ, Wang J, Liu K (2018) Sequence variation and functional analysis of a FRIGIDA orthologue (BnaAFRI) in Brassica napus. BMC Plant Biol. https://doi.org/10.1186/s12870-018-1253-1. (PMID: 10.1186/s12870-018-1253-1302680936162897)
Yin S, Wan M, Guo C, Wang B, Li H, Li G, Tian Y, Ge X, King GJ, Liu K, Li Z, Wang J (2020) Transposon insertions within alleles of BnaFLCA and BnaFLCA are associated with seasonal crop type in rapeseed. J Exper Bot 71(16):4729–4741. (PMID: 10.1093/jxb/eraa237)
Zou X, Suppanz I, Raman H, Hou J, Wang J, Long Y, Jung C, Meng J (2012) Comparative analysis of FLC homologues in brassicaceae provides insight into their role in the evolution of oilseed rape. PloS one. https://doi.org/10.1371/journal.pone.0045751. (PMID: 10.1371/journal.pone.0045751233008313531395)
Grant Information:: 2017YFD0101700 national key research and development program of china; 2662020ZKPY021 Fundamental Research Funds for the Central Universities; 2018YFD1000900 National Key Research and Development Program of China; 31471531 National Natural Science Foundation of China
Substance Nomenclature:: 0 (Plant Proteins)
0 (Transcription Factors)
Entry Date(s):: Date Created: 20210819 Date Completed: 20211001 Latest Revision: 20220426
Update Code:: 20240104
DOI:: 10.1007/s00122-021-03896-x
PMID:: 34410456
: Czasopismo naukowe

Full Text Finder

Key Message: Two CO paralogs in Brassica napus were confirmed and shown distinct expression pattern and function in promoting flowering and allelic variation s within BnaCO.A10 were found closely associated with ecotype divergence. CONSTANS (CO) is a key gene that responds to photoperiod and in Arabidopsis can promote flowering under long-day (LD) conditions. Brassica napus L. is a major oil crop and close relative of Arabidopsis, and arose via allopolyploidization from the diploids B. rapa (A genome) and B. oleracea (C genome). In this study, we confirmed that B. napus has two CO genes located on the A10 (BnaCO.A10) and C9 (BnaCO.C9) chromosomes. Significant differences in level and temporal pattern of transcription, as well as in protein function, of these homoeologous may have resulted from sequence variation in the promoter as well as in the coding region. Apart from two insertions of 527 bp and 2002 bp in the promoter of BnaCO.C9 that function as transcriptional enhancers, this gene is otherwise highly conserved in both promoter and coding region. However, BnaCO.A10 was classified into two haplotypes and transgene analysis in Arabidopsis and backcross analysis in rapeseed indicated that the winter-type haplotype had a greater effect in promoting flowering than the spring type. We discuss the contribution of CO alleles to species evolution, and for eco-geographic radiation following crop domestication, alongside scope for managing this locus in future breeding.
(© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Informacja