Home LiteratureArticle Details
PMID: 23213200 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A conserved molecular basis for photoperiod adaptation in two temperate legumes.

Weller JL, Liew LC, Hecht VF, Rajandran V, Laurie RE, Ridge S, Wenden B, Vander Schoor JK, Jaminon O, Blassiau C, Dalmais M, Rameau C, Bendahmane A, Macknight RC, Lejeune-Hénaut I

Abstract

Legumes were among the first plant species to be domesticated, and accompanied cereals in expansion of agriculture from the Fertile Crescent into diverse environments across the Mediterranean basin, Europe, Central Asia, and the Indian subcontinent. Although several recent studies have outlined the molecular basis for domestication and eco-geographic adaptation in the two main cereals from this region, wheat and barley, similar questions remain largely unexplored in their legume counterparts. Here we identify two major loci controlling differences in photoperiod response between wild and domesticated pea, and show that one of these, high response to photoperiod (HR), is an ortholog of early flowering 3 (ELF3), a gene involved in circadian clock function. We found that a significant proportion of flowering time variation in global pea germplasm is controlled by HR, with a single, widespread functional variant conferring altered circadian rhythms and the reduced photoperiod response associated with the spring habit. We also present evidence that ELF3 has a similar role in lentil, another major legume crop, with a distinct functional variant contributing to reduced photoperiod response in cultivars widely deployed in short-season environments. Our results identify the factor likely to have permitted the successful prehistoric expansion of legume cultivation to Northern Europe, and define a conserved genetic basis for major adaptive changes in flowering phenology and growth habit in an important crop group.

MeSH Terms
Acclimatization/genetics Adaptation, Physiological/genetics Circadian Clocks Circadian Rhythm/genetics Fabaceae/physiology Gene Expression Regulation, Plant Genes, Plant Genetic Variation Lens Plant/metabolism Models, Genetic Molecular Sequence Data Peas/genetics,metabolism Phenotype Photoperiod Seasons
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Weller James L
School of Plant Science, University of Tasmania, Hobart, Tasmania 7001, Australia. jim.weller@utas.edu.au
Liew Lim Chee
Hecht Valérie F G
Rajandran Vinodan
Laurie Rebecca E
Ridge Stephen
Wenden Bénédicte
Vander Schoor Jacqueline K
Jaminon Odile
Blassiau Christelle
Dalmais Marion
Rameau Catherine
Bendahmane Abdelhafid
Macknight Richard C
Lejeune-Hénaut Isabelle
References (31)
31 references, click to expand
  1. Translational Genomics in Legumes Allowed Placing In Silico 5460 Unigenes on the Pea Functional Map and Identified Candidate Genes in Pisum sativum L.
    G3 (Bethesda). 2011 Jul;1(2):93-103 PMID: 22384322
  2. FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3281-5 PMID: 14973192
  3. LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms.
    Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10387-92 PMID: 16006522
  4. The nature of selection during plant domestication.
    Nature. 2009 Feb 12;457(7231):843-8 PMID: 19212403
  5. Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley.
    Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4326-31 PMID: 22371569
  6. The wheat VRN2 gene is a flowering repressor down-regulated by vernalization.
    Science. 2004 Mar 12;303(5664):1640-4 PMID: 15016992
  7. Conservation of Arabidopsis flowering genes in model legumes.
    Plant Physiol. 2005 Apr;137(4):1420-34 PMID: 15778459
  8. DIE NEUTRALIS and LATE BLOOMER 1 contribute to regulation of the pea circadian clock.
    Plant Cell. 2009 Oct;21(10):3198-211 PMID: 19843842
  9. The ELF3 zeitnehmer regulates light signalling to the circadian clock.
    Nature. 2000 Dec 7;408(6813):716-20 PMID: 11130072
  10. Transposable elements reveal the impact of introgression, rather than transposition, in Pisum diversity, evolution, and domestication.
    Mol Biol Evol. 2003 Dec;20(12):2067-75 PMID: 12949152
  11. Characterization of responses to temperature and photoperiod for time to flowering in a world lentil collection.
    Theor Appl Genet. 1990 Aug;80(2):193-9 PMID: 24220895
  12. Arabidopsis FHY3 specifically gates phytochrome signaling to the circadian clock.
    Plant Cell. 2006 Oct;18(10):2506-16 PMID: 17012604
  13. The chickpea, summer cropping, and a new model for pulse domestication in the ancient near east.
    Q Rev Biol. 2003 Dec;78(4):435-48 PMID: 14737827
  14. Analysis of a diverse global Pisum sp. collection and comparison to a Chinese local P. sativum collection with microsatellite markers.
    Theor Appl Genet. 2009 Jan;118(2):193-204 PMID: 18815768
  15. Highly-multiplexed SNP genotyping for genetic mapping and germplasm diversity studies in pea.
    BMC Genomics. 2010 Aug 11;11:468 PMID: 20701750
  16. The pea GIGAS gene is a FLOWERING LOCUS T homolog necessary for graft-transmissible specification of flowering but not for responsiveness to photoperiod.
    Plant Cell. 2011 Jan;23(1):147-61 PMID: 21282524
  17. Network analysis identifies ELF3 as a QTL for the shade avoidance response in Arabidopsis.
    PLoS Genet. 2010 Sep 09;6(9):e1001100 PMID: 20838594
  18. Mutation detection using ENDO1: application to disease diagnostics in humans and TILLING and Eco-TILLING in plants.
    BMC Mol Biol. 2008 Apr 23;9:42 PMID: 18433472
  19. Experimental growing of wild pea in Israel and its bearing on Near Eastern plant domestication.
    Ann Bot. 2011 Jun;107(8):1399-404 PMID: 21527420
  20. FLOWERING LOCUS C-dependent and -independent regulation of the circadian clock by the autonomous and vernalization pathways.
    BMC Plant Biol. 2006 May 31;6:10 PMID: 16737527
  21. 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 May 22;109(21):8328-33 PMID: 22566625
  22. DETERMINATE and LATE FLOWERING are two TERMINAL FLOWER1/CENTRORADIALIS homologs that control two distinct phases of flowering initiation and development in pea.
    Plant Cell. 2003 Nov;15(11):2742-54 PMID: 14563931
  23. Ef7 encodes an ELF3-like protein and promotes rice flowering by negatively regulating the floral repressor gene Ghd7 under both short- and long-day conditions.
    Plant Cell Physiol. 2012 Apr;53(4):717-28 PMID: 22422935
  24. The flowering locus Hr colocalizes with a major QTL affecting winter frost tolerance in Pisum sativum L.
    Theor Appl Genet. 2008 May;116(8):1105-16 PMID: 18347775
  25. Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum.
    Proc Natl Acad Sci U S A. 2011 Sep 27;108(39):16469-74 PMID: 21930910
  26. A pseudo-response regulator is misexpressed in the photoperiod insensitive Ppd-D1a mutant of wheat (Triticum aestivum L.).
    Theor Appl Genet. 2007 Sep;115(5):721-33 PMID: 17634915
  27. The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth.
    Nature. 2011 Jul 13;475(7356):398-402 PMID: 21753751
  28. Circadian-associated rice pseudo response regulators (OsPRRs): insight into the control of flowering time.
    Biosci Biotechnol Biochem. 2005 Feb;69(2):410-4 PMID: 15725670
  29. The genetic diversity and evolution of field pea (Pisum) studied by high throughput retrotransposon based insertion polymorphism (RBIP) marker analysis.
    BMC Evol Biol. 2010 Feb 15;10:44 PMID: 20156342
  30. What has natural variation taught us about plant development, physiology, and adaptation?
    Plant Cell. 2009 Jul;21(7):1877-96 PMID: 19574434
  31. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability.
    Mol Cell. 2008 Dec 5;32(5):617-30 PMID: 19061637
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2012-12-18
Epub
2012-00-03
Pages
21158-63
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC3529011
Subset
IM
Databases
GENBANK
JN983406, JN983407
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com