Advertisement

Nulliplex-branch, a TERMINAL FLOWER 1 ortholog, controls plant growth habit in cotton

  • Wei Chen
  • Jinbo Yao
  • Yan Li
  • Lanjie Zhao
  • Jie Liu
  • Yan Guo
  • Junyi Wang
  • Li Yuan
  • Ziyang Liu
  • Youjun Lu
  • Yongshan Zhang
Original Article

Abstract

Key message

Nulliplex-branch (nb) mutants in cotton display a specific architecture. The gene responsible for the nb phenotype was identified, and its modulation mode was further studied.

Abstract

Plant architecture is an important agronomic factor influencing various traits such as yield and variety adaptability in crop plants. Cotton (Gossypium) simultaneously displays monopodial and sympodial growth. Nulliplex-branch (nb) mutants showing determinate sympodial shoots have been reported in both G. hirsutum (Ghnb) and G. barbadense (Gbnb). In this study, the gene responsible for the nb phenotype was identified. GhNB and GbNB were found to be allelic loci and are TERMINAL FLOWER 1 orthologs on the Dt subgenome, though the At copies remain native. Sequencing and association analyses identified four (Gh-nb1Gh-nb4) and one (Gb-nb1) type of point mutation in the coding sequences of Ghnb and Gbnb, respectively. The NB gene was mainly expressed in the root and shoot apex, and expression rhythms were also observed in these tissues, suggesting that the expression of the NB gene could be regulated by photoperiod. Constitutive overexpression of GhNB suppresses the differentiation of the reproductive shoots. Knockout of both copies of GhNB caused the main and lateral shoots to terminate in flowers, which is a more determinate architecture than that of the nb mutants and implies that its function might be dosage dependent. A protein lipid overlay assay indicated that the amino acid substitutions in Gh-nb1 and Gb-nb1 weaken the ligand-binding activity of the NB protein in vitro. These findings suggest that the NB gene plays crucial roles in regulating the determinacy of shoots, and the modulation of this gene should constitute an effective crop improvement approach through adjusting the growth habit of cotton.

Notes

Acknowledgements

This research was funded by the National Natural Science Foundation of China (31671740). We thank the national mid-term cotton gene bank of ICR-CAAS for providing the cotton materials.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The authors declare that the experiments comply with the current laws of China.

Supplementary material

122_2018_3197_MOESM1_ESM.docx (2.6 mb)
Supplementary material 1 (DOCX 2673 kb)
122_2018_3197_MOESM2_ESM.xlsx (51 kb)
Supplementary material 2 (XLSX 51 kb)
122_2018_3197_MOESM3_ESM.xlsx (19 kb)
Supplementary material 3 (XLSX 18 kb)

References

  1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005) FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052CrossRefGoogle Scholar
  2. Ahn JH, Miller DM, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D (2006) A divergent external loop confers antagonistic activity on floral regulators FT and TFL1. EMBO J 25:605–614CrossRefGoogle Scholar
  3. Awai K, Xu C, Tamot B, Benning C (2006) A phosphatidic acid-binding protein of the chloroplast inner envelope membrane involved in lipid trafficking. Proc Natl Acad Sci USA 103:10817–10822CrossRefGoogle Scholar
  4. Banfield MJ, Brady RL (2000) The structure of Antirrhinum centroradialis protein (CEN) suggests a role as a kinase regulator. J Mol Biol 297:1159–1170CrossRefGoogle Scholar
  5. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein SJ, Coen E (1996) Control of inflorescence architecture in Antirrhinum. Nature 379:791–797CrossRefGoogle Scholar
  6. Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E (1997) Inflorescence commitment and architecture in Arabidopsis. Science 275:80CrossRefGoogle Scholar
  7. Chen W, Yao J, Chu L, Yuan Z, Li Y, Zhang Y (2015) Genetic mapping of the nulliplex-branch gene (gb_nb1) in cotton using next-generation sequencing. Theor Appl Genet 128:539–547CrossRefGoogle Scholar
  8. Chung KS, Yoo SY, Yoo SJ, Lee JS, Ahn JH (2010) BROTHER OF FT AND TFL1 (BFT), a member of the FT/TFL1 family, shows distinct pattern of expression during the vegetative growth of Arabidopsis. Plant Signal Behav 5:1102–1104CrossRefGoogle Scholar
  9. Comadran J, Kilian B, Russell J, Ramsay L, Stein N, Ganal M, Shaw P, Bayer M, Thomas W, Marshall D (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44:1388–1392CrossRefGoogle Scholar
  10. Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030CrossRefGoogle Scholar
  11. Dowler S, Kular GS, Alessi DR (2002) Protein lipid overlay assay. Sci Signal 2002:pl6CrossRefGoogle Scholar
  12. Elitzur T, Nahum H, Borovsky Y, Pekker I, Eshed Y, Paran I (2009) Co-ordinated regulation of flowering time, plant architecture and growth by FASCICULATE: the pepper orthologue of SELF PRUNING. J Exp Bot 60:869–880CrossRefGoogle Scholar
  13. Endrizzi JE, Ray DT (1992) Mapping of the cl1, R1, yg1, and Dw loci in the long arm of chromosome 16 of cotton. J Econ Soc Hist Orient 53:778–780Google Scholar
  14. Fang L, Wang Q, Hu Y, Jia Y, Chen J, Liu B, Zhang Z, Guan X, Chen S, Zhou B, Mei G, Sun J, Pan Z, He S, Xiao S, Shi W, Gong W, Liu J, Ma J, Cai C, Zhu X, Guo W, Du X, Zhang T (2017) Genomic analyses in cotton identify signatures of selection and loci associated with fiber quality and yield traits. Nat Genet 49:1089–1098CrossRefGoogle Scholar
  15. Foucher F, Morin J, Courtiade J, Cadioux S, Ellis N, Banfield MJ, Rameau C (2003) DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea. Plant Cell 15:2742–2754CrossRefGoogle Scholar
  16. Gore UR (1935) Morphogenetic studies on the inflorescence of cotton. Bot Gaz 97:118–138CrossRefGoogle Scholar
  17. Grover CE, Gallagher JP, Jareczek JJ, Page JT, Udall JA, Gore MA, Wendel JF (2015) Re-evaluating the phylogeny of allopolyploid Gossypium L. Mol Phylogenet Evol 92:45–52CrossRefGoogle Scholar
  18. Guo D, Li C, Dong R, Li X, Xiao X, Huang X (2015) Molecular cloning and functional analysis of the FLOWERING LOCUS T (FT) homolog GhFT1 from Gossypium hirsutum. J Integr Plant Biol 57:522–533CrossRefGoogle Scholar
  19. Hanzawa Y, Money T, Bradley D (2005) A single amino acid converts a repressor to an activator of flowering. Proc Natl Acad Sci USA 102:7748–7753CrossRefGoogle Scholar
  20. Ho WW, Weigel D (2014) Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T. Plant Cell 26:552–564CrossRefGoogle Scholar
  21. Huang NC, Jane WN, Chen J, Yu TS (2012) Arabidopsis thaliana CENTRORADIALIS homologue (ATC) acts systemically to inhibit floral initiation in Arabidopsis. Plant J 72:175–184CrossRefGoogle Scholar
  22. Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60:614–625CrossRefGoogle Scholar
  23. Jia Y, Sun X, Sun J, Pan Z, Wang X, He S, Xiao S, Shi W, Zhou Z, Pang B (2014) Association Mapping for epistasis and environmental interaction of yield traits in 323 cotton cultivars under 9 different environments. PLoS ONE 9:e95882CrossRefGoogle Scholar
  24. Jin S, Zhang X, Nie Y, Guo X, Liang S, Zhu H (2006) Identification of a novel elite genotype for in vitro culture and genetic transformation of cotton. Biol Plant 50:519–524CrossRefGoogle Scholar
  25. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286:1962–1965CrossRefGoogle Scholar
  26. Kearney TH (1930) Short branch, another character of cotton showing monohybrid inheritance. J Agric Res 41:379–387Google Scholar
  27. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic Roles in mediating flowering signals. Science 286:1960–1962CrossRefGoogle Scholar
  28. Kong D, Qu L, Zhang X, Liu J, Wang P, Li F (2017) Optimization of EMS mutagenesis condition and screening of mutants in Gossypium arboretum L. Cotton Sci 29:336–344Google Scholar
  29. Koskela EA, Mouhu K, Albani MC, Kurokura T, Rantanen M, Sargent DJ, Battey NH, Coupland G, Elomaa P, Hytönen T (2012) Mutation in TERMINAL FLOWER1 reverses the photoperiodic requirement for flowering in the wild strawberry Fragaria vesca. Plant Physiol 159:1043–1054CrossRefGoogle Scholar
  30. Liu BH, Watanabe S, Uchiyama T, Kong FJ, Kanazawa A, Xia ZJ, Nagamatsu A, Arai M, Yamada T, Kitamura K (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol 153:198–210CrossRefGoogle Scholar
  31. Liu X, Zhao B, Zheng HJ, Hu Y, Lu G, Yang CQ, Chen JD, Chen JJ, Chen DY, Zhang L, Zhou Y, Wang LJ, Guo WZ, Bai YL, Ruan JX, Shangguan XX, Mao YB, Shan CM, Jiang JP, Zhu YQ, Jin L, Kang H, Chen ST, He XL, Wang R, Wang YZ, Chen J, Wang LJ, Yu ST, Wang BY, Wei J, Song SC, Lu XY, Gao ZC, Gu WY, Deng X, Ma D, Wang S, Liang WH, Fang L, Cai CP, Zhu XF, Zhou BL, Jeffrey Chen Z, Xu SH, Zhang YG, Wang SY, Zhang TZ, Zhao GP, Chen XY (2015) Gossypium barbadense genome sequence provides insight into the evolution of extra-long staple fiber and specialized metabolites. Sci Rep 5:14139CrossRefGoogle Scholar
  32. McGarry RC, Ayre BG (2012) Geminivirus-mediated delivery of florigen promotes determinate growth in aerial organs and uncouples flowering from photoperiod in cotton. PLoS ONE 7:e36746CrossRefGoogle Scholar
  33. McGarry RC, Prewitt SF, Culpepper S, Eshed Y, Lifschitz E, Ayre BG (2016) Monopodial and sympodial branching architecture in cotton is differentially regulated by the Gossypium hirsutum SINGLE FLOWER TRUSS and SELF-PRUNING orthologs. New Phytol 212:244–258CrossRefGoogle Scholar
  34. Mcsteen P, Leyser O (2005) Shoot branching. Annu Rev Plant Biol 56:353–374CrossRefGoogle Scholar
  35. Michael W, Christina C, Katia S, Oliver B, Katrin W, Christian N, Dragica B, Christopher G, Karin S, Claudia O (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40:428–438CrossRefGoogle Scholar
  36. Mimida N, Goto K, Kobayashi Y, Araki T, Ahn JH, Weigel D, Murata M, Motoyoshi F, Sakamoto W (2001) Functional divergence of the TFL1-like gene family in Arabidopsis revealed by characterization of a novel homologue. Genes Cells 6:327–336CrossRefGoogle Scholar
  37. Nakagawa M, Shimamoto K, Kyozuka J (2002) Overexpression of RCN1 and RCN2, rice TERMINAL FLOWER 1/CENTRORADIALIS homologs, confers delay of phase transition and altered panicle morphology in rice. Plant J Cell Mol Biol 29:743–750CrossRefGoogle Scholar
  38. Nakamura Y, Andres F, Kanehara K, Liu YC, Dormann P, Coupland G (2014) Arabidopsis florigen FT binds to diurnally oscillating phospholipids that accelerate flowering. Nat Commun 5:3553CrossRefGoogle Scholar
  39. Park SJ, Jiang K, Tal L, Yichie Y, Gar O, Zamir D, Eshed Y, Lippman ZB (2014) Optimization of crop productivity in tomato using induced mutations in the florigen pathway. Nat Genet 46:1337–1342CrossRefGoogle Scholar
  40. Patel GB, Munshi ZA, Patel CT (1947) Mutation in Gujrat Cotton (Gossypium herbaceum). In: Indian Central Cotton Committee, 3rd conferenceGoogle Scholar
  41. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin D, Llewellyn D, Showmaker KC, Shu S, Udall J, Yoo MJ, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover C, Grupp K, Hu G, Lee TH, Li J, Lin L, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, Tan X, Tang H, Xu C, Wang J, Wang Z, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers JE, Brubaker CL, Chee PW, Das S, Gingle AR, Haigler CH, Harker D, Hoffmann LV, Hovav R, Jones DC, Lemke C, Mansoor S, ur Rahman M, Rainville LN, Rambani A, Reddy UK, Rong JK, Saranga Y, Scheffler BE, Scheffler JA, Stelly DM, Triplett BA, Van Deynze A, Vaslin MF, Waghmare VN, Walford SA, Wright RJ, Zaki EA, Zhang T, Dennis ES, Mayer KF, Peterson DG, Rokhsar DS, Wang X, Schmutz J (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427CrossRefGoogle Scholar
  42. Pathak RS, Singh RB (1975) Genetic analysis of the duplicate loci, cluster and short branch in Gossypium hirsutum L. Theor Appl Genet 46:281PubMedGoogle Scholar
  43. Pnueli L, Carmel-Goren L, Hareven D, Gutfinger T, Alvarez J, Ganal M, Zamir D, Lifschitz E (1998) The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1. Development 125:1979–1989PubMedGoogle Scholar
  44. Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N, Adir N, Lifschitz E (2001) Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell 13:2687–2702CrossRefGoogle Scholar
  45. 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 80:847–857CrossRefGoogle Scholar
  46. Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ (1998) A common mechanism controls the life cycle and architecture of plants. Development 125:1609PubMedGoogle Scholar
  47. Reinhardt D, Kuhlemeier C (2002) Plant architecture. EMBO Rep 3:846–851CrossRefGoogle Scholar
  48. 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 288:1613–1616CrossRefGoogle Scholar
  49. Schütze K, Harter K, Chaban C (2009) Bimolecular Fluorescence Complementation (BiFC) to study srotein-protein interactions in living plant cells. In: Pfannschmidt T (ed) Plant signal transduction: methods and protocols. Humana Press, Totowa, pp 189–202CrossRefGoogle Scholar
  50. Shannon S, Meeks-Wagner DR (1991) A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 3:877–892CrossRefGoogle Scholar
  51. Silow RA (1946) Evidence on chromosome homology and gene homology in the amphidiploid new world cottons. J Genet 47:213–221CrossRefGoogle Scholar
  52. Song Q, Zhang T, Stelly DM, Chen ZJ (2017) Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol 18:99CrossRefGoogle Scholar
  53. Soyk S, Müller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van EJ, Jiménez-Gómez JM, Lippman ZB (2017) Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato. Nat Genet 49:162CrossRefGoogle Scholar
  54. Stephens SG (1955) Linkage in upland cotton. Genetics 40:903PubMedPubMedCentralGoogle Scholar
  55. Sun Q, Du X, Cai C, Long L, Zhang S, Qiao P, Wang W, Zhou K, Wang G, Liu X, Zhang H, Geng S, Yang C, Gao W, Mo J, Miao C, Song C, Cai Y (2016) To be a flower or fruiting branch: insights revealed by mRNA and small RNA transcriptomes from different cotton developmental stages. Sci Rep 6:23212CrossRefGoogle Scholar
  56. Tian Z, Wang X, Lee R, Li Y, Specht JE, Nelson RL, Mcclean PE, Qiu L, Ma J (2010) Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci USA 107:8563CrossRefGoogle Scholar
  57. Wang Y, Li J (2006) Genes controlling plant architecture. Curr Opin Biotechnol 17:123–129CrossRefGoogle Scholar
  58. Wang L, Zhu Y, Hu W, Zhang X, Cai C, Guo W (2015) Comparative transcriptomics reveals jasmonic acid-associated metabolism related to cotton fiber initiation. PLoS ONE 10:e0129854CrossRefGoogle Scholar
  59. Wang M, Tu L, Lin M, Lin Z, Wang P, Yang Q, Ye Z, Shen C, Li J, Zhang L, Zhou X, Nie X, Li Z, Guo K, Ma Y, Huang C, Jin S, Zhu L, Yang X, Min L, Yuan D, Zhang Q, Lindsey K, Zhang X (2017a) Asymmetric subgenome selection and cis-regulatory divergence during cotton domestication. Nat Genet 49:579–587CrossRefGoogle Scholar
  60. Wang P, Zhang J, Sun L, Ma Y, Xu J, Liang S, Deng J, Tan J, Zhang Q, Tu L (2017b) High efficient multi-sites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnol J 16:137–150CrossRefGoogle Scholar
  61. Wang Y, Yu H, Tian C, Sajjad M, Gao C, Tong Y, Wang X, Jiao Y (2017c) Transcriptome association identifies regulators of wheat spike architecture. Plant Physiol 175:746–757CrossRefGoogle Scholar
  62. Wendel JF, Cronn RC (2003) Polyploidy and the evolutionary history of cotton. Adv Agron 78:139–186CrossRefGoogle Scholar
  63. Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8:983–997CrossRefGoogle Scholar
  64. Wigge PA, Min CK, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059CrossRefGoogle Scholar
  65. Yamaguchi A, Kobayashi Y, Goto K, Abe M, Araki T (2005) TWIN SISTER OF FT (TSF) acts as a floral pathway integrator redundantly with FT. Plant Cell Physiol 46:1175–1189CrossRefGoogle Scholar
  66. Yuan D, Tang Z, Wang M, Gao W, Tu L, Jin X, Chen L, He Y, Zhang L, Zhu L, Li Y, Liang Q, Lin Z, Yang X, Liu N, Jin S, Lei Y, Ding Y, Li G, Ruan X, Ruan Y, Zhang X (2015) The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres. Sci Rep 5:17662CrossRefGoogle Scholar
  67. Zhai XJ, Li YY, Wang YL, Gong RP, Zhai LF, Shi XY (2011) Transgenic insect-resistant short-season cotton cultivars, Xiazao 2 and Xiazao 3. China Cotton 38:34–35Google Scholar
  68. Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–537CrossRefGoogle Scholar
  69. Zhang X, Wang C, Pang C, Wei H, Wang H, Song M, Fan S, Yu S (2016a) Characterization and functional analysis of PEBP family genes in upland cotton (Gossypium hirsutum L.). PLoS ONE 11:e0161080CrossRefGoogle Scholar
  70. Zhang YN, Cai DR, Huang XZ (2016b) Identification of bZIP protein family in Gossypium arboreum and tissue expression analysis of GaFDs genes. Acta Agron Sin 42:832CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Cotton Biology, Institute of Cotton ResearchChinese Academy of Agricultural SciencesAnyangChina
  2. 2.Art and Science CollegeUniversity of SaskatchewanSaskatoonCanada

Personalised recommendations