Epistatic interactions between PHOTOPERIOD1, CONSTANS1 and CONSTANS2 modulate the photoperiodic response in wheat
Autoři:
Lindsay M. Shaw aff001; Chengxia Li aff001; Daniel P. Woods aff001; Maria A. Alvarez aff001; Huiqiong Lin aff001; Mei Y. Lau aff001; Andrew Chen aff001; Jorge Dubcovsky aff001
Působiště autorů:
Department of Plant Sciences, University of California, Davis, California, United States of America
aff001; Currently at Queensland Alliance for Agriculture and Food Innovation, The University of Queensland, Brisbane, QLD, Australia
aff002; Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America
aff003
Vyšlo v časopise:
Epistatic interactions between PHOTOPERIOD1, CONSTANS1 and CONSTANS2 modulate the photoperiodic response in wheat. PLoS Genet 16(7): e32767. doi:10.1371/journal.pgen.1008812
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008812
Souhrn
In Arabidopsis, CONSTANS (CO) integrates light and circadian clock signals to promote flowering under long days (LD). In the grasses, a duplication generated two paralogs designated as CONSTANS1 (CO1) and CONSTANS2 (CO2). Here we show that in tetraploid wheat plants grown under LD, combined loss-of-function mutations in the A and B-genome homeologs of CO1 and CO2 (co1 co2) result in a small (3 d) but significant (P<0.0001) acceleration of heading time both in PHOTOPERIOD1 (PPD1) sensitive (Ppd-A1b, functional ancestral allele) and insensitive (Ppd-A1a, functional dominant allele) backgrounds. Under short days (SD), co1 co2 mutants headed 13 d earlier than the wild type (P<0.0001) in the presence of Ppd-A1a. However, in the presence of Ppd-A1b, spikes from both genotypes failed to emerge by 180 d. These results indicate that CO1 and CO2 operate mainly as weak heading time repressors in both LD and SD. By contrast, in ppd1 mutants with loss-of-function mutations in both PPD1 homeologs, the wild type Co1 allele accelerated heading time >60 d relative to the co1 mutant allele under LD. We detected significant genetic interactions among CO1, CO2 and PPD1 genes on heading time, which were reflected in complex interactions at the transcriptional and protein levels. Loss-of-function mutations in PPD1 delayed heading more than combined co1 co2 mutations and, more importantly, PPD1 was able to perceive and respond to differences in photoperiod in the absence of functional CO1 and CO2 genes. Similarly, CO1 was able to accelerate heading time in response to LD in the absence of a functional PPD1. Taken together, these results indicate that PPD1 and CO1 are able to respond to photoperiod in the absence of each other, and that interactions between these two photoperiod pathways at the transcriptional and protein levels are important to fine-tune the flowering response in wheat.
Klíčová slova:
Arabidopsis thaliana – Flowering plants – Leaves – Mutation – Protein interactions – Rice – Transcriptional control – Wheat
Zdroje
1. Bouche F, Woods DP, Amasino RM. Winter memory throughout the plant kingdom: different paths to flowering. Plant Physiol. 2017;173(1):27–35. doi: 10.1104/pp.16.01322 27756819.
2. Garner WW, Allard HA. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J Agric Res. 1919;18:0553–606.
3. Andres F, Coupland G. The genetic basis of flowering responses to seasonal cues. Nat Rev Genet. 2012;13(9):627–39. doi: 10.1038/nrg3291 22898651.
4. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature. 2001;410(6832):1116–20. doi: 10.1038/35074138 11323677
5. Yanovsky MJ, Kay SA. Molecular basis of seasonal time measurement in Arabidopsis. Nature. 2002;419(6904):308–12. doi: 10.1038/nature00996 12239570.
6. Putterill J, Robson F, Lee K, Simon R, Coupland G. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell. 1995;80(6):847–57. doi: 10.1016/0092-8674(95)90288-0 7697715.
7. Griffiths S, Dunford RP, Coupland G, Laurie DA. The evolution of CONSTANS-like gene families in barley, rice, and Arabidopsis. Plant Physiol. 2003;131(4):1855–67. doi: 10.1104/pp.102.016188 12692345.
8. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, et al. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell. 2000;12(12):2473–84. doi: 10.1105/tpc.12.12.2473 11148291.
9. Higgins JA, Bailey PC, Laurie DA. Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS One. 2010;5(4):e10065. doi: 10.1371/journal.pone.0010065 20419097.
10. Campoli C, Drosse B, Searle I, Coupland G, von Korff M. Functional characterisation of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J. 2012;69(5):868–80. doi: 10.1111/j.1365-313X.2011.04839.x 22040323.
11. Mulki MA, von Korff M. CONSTANS controls floral repression by up-regulating VERNALIZATION2 (VRN-H2) in Barley. Plant Physiol. 2016;170(1):325–37. doi: 10.1104/pp.15.01350 26556793.
12. Turner A, Beales J, Faure S, Dunford RP, Laurie DA. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science. 2005;310(5750):1031–4. doi: 10.1126/science.1117619 16284181.
13. Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, et al. Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant. 2013;6(6):1877–88. doi: 10.1093/mp/sst088 23713079.
14. Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, et al. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci U S A. 2011;108(39):16469–74. doi: 10.1073/pnas.1106212108 21930910.
15. Chen A, Li C, Hu W, Lau MY, Lin H, Rockwell NC, et al. Phytochrome C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc Natl Acad Sci U S A. 2014;111(28):10037–44. doi: 10.1073/pnas.1409795111 24961368.
16. Beales J, Turner A, Griffiths S, Snape JW, Laurie DA. A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.). Theor Appl Genet. 2007;115(5):721–33. doi: 10.1007/s00122-007-0603-4 17634915.
17. Wilhelm EP, Turner AS, Laurie DA. Photoperiod insensitive Ppd-A1a mutations in tetraploid wheat (Triticum durum Desf.). Theor Appl Genet. 2009;118(2):285–94. doi: 10.1007/s00122-008-0898-9 18839130.
18. Pearce S, Vanzetti LS, Dubcovsky J. Exogenous gibberellins induce wheat spike development under short days only in the presence of VERNALIZATION1. Plant Physiol. 2013;163(3):1433–45. doi: 10.1104/pp.113.225854 24085801.
19. Pearce S, Shaw LM, Lin H, Cotter JD, Li C, Dubcovsky J. Night-break experiments shed light on the Photoperiod1-mediated flowering. Plant Physiol. 2017;174(2):1139–50. doi: 10.1104/pp.17.00361 28408541.
20. Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L. Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol. 2006;60:469–80. doi: 10.1007/s11103-005-4814-2 16525885
21. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, et al. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science. 2004;303(5664):1640–4. doi: 10.1126/science.1094305 15016992.
22. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J. Positional cloning of wheat vernalization gene VRN1. Proc Natl Acad Sci USA. 2003;100:6263–8. doi: 10.1073/pnas.0937399100
23. Chen A, Dubcovsky J. Wheat TILLING mutants show that the vernalization gene VRN1 down-regulates the flowering repressor VRN2 in leaves but is not essential for flowering. PLoS Genet. 2012;8(12):e1003134. doi: 10.1371/journal.pgen.1003134 23271982.
24. Shaw LM, Turner AS, Herry L, Griffiths S, Laurie DA. Mutant alleles of Photoperiod-1 in wheat (Triticum aestivum L.) that confer a late flowering phenotype in long days. PLoS One. 2013;8(11):e79459. doi: 10.1371/journal.pone.0079459 24244507.
25. Krasileva KV, Vasquez-Gross HA, Howell T, Bailey P, Paraiso F, Clissold L, et al. Uncovering hidden variation in polyploid wheat. Proc Natl Acad Sci U S A. 2017;114(6):E913–E21. doi: 10.1073/pnas.1619268114 28096351.
26. Uauy C, Paraiso F, Colasuonno P, Tran RK, Tsai H, Berardi S, et al. A modified TILLING approach to detect induced mutations in tetraploid and hexaploid wheat. BMC Plant Biol. 2009;9:115. doi: 10.1186/1471-2229-9-115 19712486.
27. Valverde F. CONSTANS and the evolutionary origin of photoperiodic timing of flowering. J Exp Bot. 2011;62(8):2453–63. doi: 10.1093/jxb/erq449 21239381.
28. Waddington SR, Cartwright PM, Wall PC. A quantitative scale of spike initial and pistil development in barley and wheat. Ann Bot-London. 1983;51(1):119–30.
29. Alvarez MA, Tranquilli G, Lewis S, Kippes N, Dubcovsky J. Genetic and physical mapping of the earliness per se locus Eps-Am1 in Triticum monococcum identifies EARLY FLOWERING 3 (ELF3) as a candidate gene. Funct Integr Genomic. 2016;16(4):365–82. doi: 10.1007/s10142-016-0490-3
30. Distelfeld A, Tranquilli G, Li C, Yan L, Dubcovsky J. Genetic and molecular characterization of the VRN2 loci in tetraploid wheat. Plant Physiol. 2009;149(1):245–57. doi: 10.1104/pp.108.129353 19005084.
31. Pearce S, Kippes N, Chen A, Debernardi JM, Dubcovsky J. RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways. BMC Plant Biol. 2016;16(1):141. doi: 10.1186/s12870-016-0831-3 27329140.
32. Kippes N, van Gessel C, Hamilton J, Akpinar A, Budak H, Dubcovsky J, et al. Effect of phyB and phyC loss-of-function mutations on wheat transcriptome under short and long day photoperiods. BMC Plant Biol. 2020; 20: 297. https://doi.org/10.1186/s12870-020-02506-0.
33. Li C, Distelfeld A, Comis A, Dubcovsky J. Wheat flowering repressor VRN2 and promoter CO2 compete for interactions with NUCLEAR FACTOR-Y complexes. Plant J. 2011;67(5):763–73. doi: 10.1111/j.1365-313X.2011.04630.x 21554456.
34. Faure S, Turner AS, Gruszka D, Christodoulou V, Davis SJ, von Korff M, et al. Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proc Natl Acad Sci U S A. 2012;109(21):8328–33. doi: 10.1073/pnas.1120496109 22566625.
35. Gao M, Geng F, Klose C, Staudt A-M, Huang H, Nguyen D, et al. Phytochromes measure photoperiod in Brachypodium. bioRxiv. 2019. doi: 10.1101/697169
36. Diaz A, Zikhali M, Turner AS, Isaac P, Laurie DA. Copy number variation affecting the Photoperiod-B1 and Vernalization-A1 genes is associated with altered flowering time in wheat (Triticum aestivum). PLoS One. 2012;7(3):e33234. doi: 10.1371/journal.pone.0033234 22457747.
37. Stracke S, Haseneyer G, Veyrieras JB, Geiger HH, Sauer S, Graner A, et al. Association mapping reveals gene action and interactions in the determination of flowering time in barley. Theor Appl Genet. 2009;118(2):259–73. doi: 10.1007/s00122-008-0896-y 18830577.
38. Alqudah AM, Sharma R, Pasam RK, Graner A, Kilian B, Schnurbusch T. Genetic dissection of photoperiod response based on GWAS of pre-anthesis phase duration in spring barley. PLoS One. 2014;9(11):e113120. doi: 10.1371/journal.pone.0113120 25420105.
39. Casto AL, Mattison AJ, Olson SN, Thakran M, Rooney WL, Mullet JE. Maturity2, a novel regulator of flowering time in Sorghum bicolor, increases expression of SbPRR37 and SbCO in long days delaying flowering. PLoS One. 2019;14(4):e0212154. doi: 10.1371/journal.pone.0212154 30969968.
40. Yang S, Murphy RL, Morishige DT, Klein PE, Rooney WL, Mullet JE. Sorghum phytochrome B inhibits flowering in long days by activating expression of SbPRR37 and SbGHD7, repressors of SbEHD1, SbCN8 and SbCN12. PLoS One. 2014;9(8):e105352. doi: 10.1371/journal.pone.0105352 25122453.
41. Yang S, Weers BD, Morishige DT, Mullet JE. CONSTANS is a photoperiod regulated activator of flowering in sorghum. BMC Plant Biol. 2014;14:148. doi: 10.1186/1471-2229-14-148 24884377.
42. Nemoto Y, Kisaka M, Fuse T, Yano M, Ogihara Y. Characterization and functional analysis of three wheat genes with homology to the CONSTANS flowering time gene in transgenic rice. Plant J. 2003;36(1):82–93. doi: 10.1046/j.1365-313x.2003.01859.x 12974813.
43. Woods DP, McKeown MA, Dong Y, Preston JC, Amasino RM. Evolution of VRN2/Ghd7-like genes in vernalization-mediated repression of grass flowering. Plant Physiol. 2016;170(4):2124–35. doi: 10.1104/pp.15.01279 26848096.
44. Fujino K, Yamanouchi U, Nonoue Y, Obara M, Yano M. Switching genetic effects of the flowering time gene Hd1 in LD conditions by Ghd7 and OsPRR37 in rice. Breeding Sci. 2019;69(1):127–32. doi: 10.1270/jsbbs.18060 31086490.
45. Zhang Z, Hu W, Shen G, Liu H, Hu Y, Zhou X, et al. Alternative functions of Hd1 in repressing or promoting heading are determined by Ghd7 status under long-day conditions. Sci Rep-Uk. 2017;7(1):5388. doi: 10.1038/s41598-017-05873-1 28710485.
46. Zhang B, Liu H, Qi F, Zhang Z, Li Q, Han Z, et al. Genetic interactions among Ghd7, Ghd8, OsPRR37 and Hd1 contribute to large variation in heading date in rice. Rice (N Y). 2019;12(1):48. doi: 10.1186/s12284-019-0314-x 31309345.
47. Maurer A, Draba V, Jiang Y, Schnaithmann F, Sharma R, Schumann E, et al. Modelling the genetic architecture of flowering time control in barley through nested association mapping. BMC Genomics. 2015;16:290. doi: 10.1186/s12864-015-1459-7 25887319.
48. Shaw LM, Turner AS, Laurie DA. The impact of photoperiod insensitive Ppd-1a mutations on the photoperiod pathway across the three genomes of hexaploid wheat (Triticum aestivum). Plant J. 2012;71(1):71–84. doi: 10.1111/j.1365-313X.2012.04971.x 22372488.
49. Qin Z, Bai Y, Muhammad S, Wu X, Deng P, Wu J, et al. Divergent roles of FT-like 9 in flowering transition under different day lengths in Brachypodium distachyon. Nat Commun. 2019;10(1):812. doi: 10.1038/s41467-019-08785-y 30778068.
50. Wang P, Gong R, Yang Y, Yu S. Ghd8 controls rice photoperiod sensitivity by forming a complex that interacts with Ghd7. BMC Plant Biol. 2019;19(1):462. doi: 10.1186/s12870-019-2053-y 31675987.
51. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, et al. The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci U S A. 2006;103(51):19581–6. doi: 10.1073/pnas.0607142103 17158798.
52. Deng W, Casao MC, Wang P, Sato K, Hayes PM, Finnegan EJ, et al. Direct links between the vernalization response and other key traits of cereal crops. Nat Commun. 2015;6:5882. doi: 10.1038/ncomms6882 25562483.
53. Li C, Lin H, Dubcovsky J. Factorial combinations of protein interactions generate a multiplicity of florigen activation complexes in wheat and barley. Plant J. 2015;84:70–82. doi: 10.1111/tpj.12960 26252567
54. Turner AS, Faure S, Zhang Y, Laurie DA. The effect of day-neutral mutations in barley and wheat on the interaction between photoperiod and vernalization. Theor Appl Genet. 2013;126(9):2267–77. doi: 10.1007/s00122-013-2133-6 23737074.
55. Hayama R, Sarid-Krebs L, Richter R, Fernandez V, Jang S, Coupland G. PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. Embo J. 2017;36(7):904–18. doi: 10.15252/embj.201693907 28270524.
56. Nakamichi N, Kita M, Ito S, Yamashino T, Mizuno T. PSEUDO-RESPONSE REGULATORS, PRR9, PRR7 and PRR5, together play essential roles close to the circadian clock of Arabidopsis thaliana. Plant Cell Physiol. 2005;46(5):686–98. doi: 10.1093/pcp/pci086 15767265.
57. Murakami M, Tago Y, Yamashino T, Mizuno T. Characterization of the rice circadian clock-associated pseudo-response regulators in Arabidopsis thaliana. Biosci Biotech Bioch. 2007;71(4):1107–10. doi: 10.1271/bbb.70048 17420570.
58. Campoli C, Shtaya M, Davis SJ, von Korff M. Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biol. 2012;12:97. doi: 10.1186/1471-2229-12-97 22720803.
59. Ben-Naim O, Eshed R, Parnis A, Teper-Bamnolker P, Shalit A, Coupland G, et al. The CCAAT binding factor can mediate interactions between CONSTANS-like proteins and DNA. Plant J. 2006;46(3):462–76. doi: 10.1111/j.1365-313X.2006.02706.x 16623906.
60. Kumimoto RW, Adam L, Hymus GJ, Repetti PP, Reuber TL, Marion CM, et al. The Nuclear Factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta. 2008;228(5):709–23. doi: 10.1007/s00425-008-0773-6 18600346.
61. Wenkel S, Turck F, Singer K, Gissot L, Le Gourrierec J, Samach A, et al. CONSTANS and the CCAAT box binding complex share a functionally important domain and interact to regulate flowering of Arabidopsis. Plant Cell. 2006;18(11):2971–84. doi: 10.1105/tpc.106.043299 17138697.
62. Woods DP, Ream TS, Minevich G, Hobert O, Amasino RM. PHYTOCHROME C is an essential light receptor for photoperiodic flowering in the temperate grass, Brachypodium distachyon. Genetics. 2014;198(1):397–408. doi: 10.1534/genetics.114.166785 25023399.
63. Osugi A, Itoh H, Ikeda-Kawakatsu K, Takano M, Izawa T. Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol. 2011;157(3):1128–37. doi: 10.1104/pp.111.181792 21880933.
64. Zheng T, Sun J, Zhou S, Chen S, Lu J, Cui S, et al. Post-transcriptional regulation of Ghd7 protein stability by phytochrome and OsGI in photoperiodic control of flowering in rice. New Phytol. 2019;224(1):306–20. doi: 10.1111/nph.16010 31225911.
65. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science. 2004;303(5660):1003–6. doi: 10.1126/science.1091761 14963328.
66. Hayama R, Coupland G. The molecular basis of diversity in the photoperiodic flowering responses of Arabidopsis and rice. Plant Physiol. 2004;135(2):677–84. doi: 10.1104/pp.104.042614 15208414
67. Krasileva KV, Buffalo V, Bailey P, Pearce S, Ayling S, Tabbita F, et al. Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol. 2013;14(6):R66. doi: 10.1186/gb-2013-14-6-r66 23800085.
68. Shan Q, Wang Y, Li J, Gao C. Genome editing in rice and wheat using the CRISPR/Cas system. Nat Protoc. 2014;9(10):2395–410. doi: 10.1038/nprot.2014.157 25232936.
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