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PMID: 27918538 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato.

Nature genetics ·Vol. 49 ·No. 1 ·2017-00-00 ·Pages 162-168

Soyk S, Müller NA, Park SJ, Schmalenbach I, Jiang K, Hayama R, Zhang L, Van Eck J, Jiménez-Gómez JM, Lippman ZB

Abstract

Plants evolved so that their flowering is triggered by seasonal changes in day length. However, day-length sensitivity in crops limits their geographical range of cultivation, and thus modification of the photoperiod response was critical for their domestication. Here we show that loss of day-length-sensitive flowering in tomato was driven by the florigen paralog and flowering repressor SELF-PRUNING 5G (SP5G). SP5G expression is induced to high levels during long days in wild species, but not in cultivated tomato because of cis-regulatory variation. CRISPR/Cas9-engineered mutations in SP5G cause rapid flowering and enhance the compact determinate growth habit of field tomatoes, resulting in a quick burst of flower production that translates to an early yield. Our findings suggest that pre-existing variation in SP5G facilitated the expansion of cultivated tomato beyond its origin near the equator in South America, and they provide a compelling demonstration of the power of gene editing to rapidly improve yield traits in crop breeding.

MeSH Terms
CRISPR-Cas Systems Flowers/genetics,growth & development Gene Expression Regulation, Plant Lycopersicon esculentum/genetics,growth & development Mutation/genetics Phenotype Plant Proteins/antagonists & inhibitors,genetics,metabolism Plants, Genetically Modified/genetics,growth & development Regulatory Sequences, Nucleic Acid/genetics Time Factors
Chemicals
Plant Proteins
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Soyk Sebastian
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
Müller Niels A
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
Park Soon Ju
Division of Biological Sciences, Wonkwang University, Iksan, Republic of Korea.
Schmalenbach Inga
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
Jiang Ke
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
Hayama Ryosuke
Department of Plant Developmental Biology, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
Zhang Lei
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany.
Van Eck Joyce
The Boyce Thompson Institute, Ithaca, New York, USA.
Jiménez-Gómez José M ORCID
Department of Plant Breeding and Genetics, Max Planck Institute for Plant Breeding Research, Cologne, Germany. | Institut Jean-Pierre Bourgin, INRA, AgroParisTech, CNRS, Université Paris-Saclay, Versailles, France.
Lippman Zachary B
Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.
References (56)
56 references, click to expand
  1. CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis.
    Nature. 2001 Apr 26;410(6832):1116-20 PMID: 11323677
  2. Molecular and geographic evolutionary support for the essential role of GIGANTEAa in soybean domestication of flowering time.
    BMC Evol Biol. 2016 Apr 12;16:79 PMID: 27072125
  3. Genetic variation in four maturity genes affects photoperiod insensitivity and PHYA-regulated post-flowering responses of soybean.
    BMC Plant Biol. 2013 Jun 25;13:91 PMID: 23799885
  4. Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system.
    Plant Physiol. 2014 Nov;166(3):1292-7 PMID: 25225186
  5. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element.
    New Phytol. 2010 Jul;187(1):57-66 PMID: 20406410
  6. A quantitative genetic basis for leaf morphology in a set of precisely defined tomato introgression lines.
    Plant Cell. 2013 Jul;25(7):2465-81 PMID: 23872539
  7. The role of recently derived FT paralogs in sunflower domestication.
    Curr Biol. 2010 Apr 13;20(7):629-35 PMID: 20303265
  8. Rate of meristem maturation determines inflorescence architecture in tomato.
    Proc Natl Acad Sci U S A. 2012 Jan 10;109(2):639-44 PMID: 22203998
  9. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice.
    Nat Genet. 2008 Jun;40(6):761-7 PMID: 18454147
  10. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato.
    Nat Genet. 2010 May;42(5):459-63 PMID: 20348958
  11. Genome editing. The new frontier of genome engineering with CRISPR-Cas9.
    Science. 2014 Nov 28;346(6213):1258096 PMID: 25430774
  12. Natural variation of the RICE FLOWERING LOCUS T 1 contributes to flowering time divergence in rice.
    PLoS One. 2013 Oct 01;8(10):e75959 PMID: 24098411
  13. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.
    Genome Biol. 2013 Apr 25;14(4):R36 PMID: 23618408
  14. 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen.
    Nature. 2011 Jul 31;476(7360):332-5 PMID: 21804566
  15. Florigen and anti-florigen - a systemic mechanism for coordinating growth and termination in flowering plants.
    Front Plant Sci. 2014 Sep 16;5:465 PMID: 25278944
  16. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering.
    Science. 2004 Feb 13;303(5660):1003-6 PMID: 14963328
  17. Genealogy and fine mapping of obscuravenosa, a gene affecting the distribution of chloroplasts in leaf veins, and evidence of selection during breeding of tomatoes (Lycopersicon esculentum; Solanaceae).
    Am J Bot. 2007 Jun;94(6):935-47 PMID: 21636462
  18. The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry.
    Plant J. 2012 Jan;69(1):116-25 PMID: 21895811
  19. The genetic basis of flowering responses to seasonal cues.
    Nat Rev Genet. 2012 Sep;13(9):627-39 PMID: 22898651
  20. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.
    Mol Biol Evol. 2013 Dec;30(12):2725-9 PMID: 24132122
  21. Fast track assembly of multigene constructs using Golden Gate cloning and the MoClo system.
    Bioeng Bugs. 2012 Jan 1;3(1):38-43 PMID: 22126803
  22. Optimization of crop productivity in tomato using induced mutations in the florigen pathway.
    Nat Genet. 2014 Dec;46(12):1337-42 PMID: 25362485
  23. The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution.
    New Phytol. 2010 Apr;186(1):54-62 PMID: 19925558
  24. Editing plant genomes with CRISPR/Cas9.
    Curr Opin Biotechnol. 2015 Apr;32:76-84 PMID: 25437637
  25. The genome of the stress-tolerant wild tomato species Solanum pennellii.
    Nat Genet. 2014 Sep;46(9):1034-8 PMID: 25064008
  26. The SELF-PRUNING gene of tomato regulates vegetative to reproductive switching of sympodial meristems and is the ortholog of CEN and TFL1.
    Development. 1998 Jun;125(11):1979-89 PMID: 9570763
  27. Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice.
    Genes Dev. 2002 Aug 1;16(15):2006-20 PMID: 12154129
  28. Tomato yield heterosis is triggered by a dosage sensitivity of the florigen pathway that fine-tunes shoot architecture.
    PLoS Genet. 2013;9(12):e1004043 PMID: 24385931
  29. A clarified position for Solanum lycopersicum var. cerasiforme in the evolutionary history of tomatoes (solanaceae).
    BMC Plant Biol. 2008 Dec 20;8:130 PMID: 19099601
  30. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley.
    Science. 2005 Nov 11;310(5750):1031-4 PMID: 16284181
  31. Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice.
    Mol Genet Genomics. 2011 Jun;285(6):461-70 PMID: 21512732
  32. Induced and natural variation of promoter length modulates the photoperiodic response of FLOWERING LOCUS T.
    Nat Commun. 2014 Aug 04;5:4558 PMID: 25087553
  33. Revisiting the involvement of SELF-PRUNING in the sympodial growth of tomato.
    Plant Physiol. 2008 Sep;148(1):61-4 PMID: 18772352
  34. Comparative genomics and phylogenetic discordance of cultivated tomato and close wild relatives.
    PeerJ. 2015 Feb 26;3:e793 PMID: 25780758
  35. An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet.
    Science. 2010 Dec 3;330(6009):1397-400 PMID: 21127254
  36. Phylogenomics Reveals Three Sources of Adaptive Variation during a Rapid Radiation.
    PLoS Biol. 2016 Feb 12;14(2):e1002379 PMID: 26871574
  37. Four Tomato FLOWERING LOCUS T-Like Proteins Act Antagonistically to Regulate Floral Initiation.
    Front Plant Sci. 2016 Jan 11;6:1213 PMID: 26793202
  38. An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL.
    Genetics. 1995 Nov;141(3):1147-62 PMID: 8582620
  39. Potato StCONSTANS-like1 Suppresses Storage Organ Formation by Directly Activating the FT-like StSP5G Repressor.
    Curr Biol. 2016 Apr 4;26(7):872-81 PMID: 26972319
  40. The tomato genome sequence provides insights into fleshy fruit evolution.
    Nature. 2012 May 30;485(7400):635-41 PMID: 22660326
  41. Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering.
    Plant Cell. 2001 Dec;13(12):2687-702 PMID: 11752381
  42. Structural features determining flower-promoting activity of Arabidopsis FLOWERING LOCUS T.
    Plant Cell. 2014 Feb;26(2):552-64 PMID: 24532592
  43. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis.
    Science. 2007 Oct 12;318(5848):261-5 PMID: 17872410
  44. Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice.
    Proc Natl Acad Sci U S A. 2009 Mar 17;106(11):4555-60 PMID: 19246394
  45. Domestication selected for deceleration of the circadian clock in cultivated tomato.
    Nat Genet. 2016 Jan;48(1):89-93 PMID: 26569124
  46. Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley.
    Nat Genet. 2012 Dec;44(12):1388-92 PMID: 23160098
  47. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1.
    EMBO J. 2006 Feb 8;25(3):605-14 PMID: 16424903
  48. The FT-like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize.
    Plant Cell. 2011 Mar;23(3):942-60 PMID: 21441432
  49. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli.
    Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6398-403 PMID: 16606827
  50. QTL analysis of transgressive segregation in an interspecific tomato cross.
    Genetics. 1993 Jun;134(2):585-96 PMID: 8100788
  51. Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis.
    Plant Cell. 2013 Mar;25(3):820-33 PMID: 23543784
  52. QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations.
    Plant J. 2013 Apr;74(1):174-83 PMID: 23289725
  53. 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
  54. The flowering hormone florigen functions as a general systemic regulator of growth and termination.
    Proc Natl Acad Sci U S A. 2009 May 19;106(20):8392-7 PMID: 19416824
  55. Naturally occurring allele diversity allows potato cultivation in northern latitudes.
    Nature. 2013 Mar 14;495(7440):246-50 PMID: 23467094
  56. A single amino acid converts a repressor to an activator of flowering.
    Proc Natl Acad Sci U S A. 2005 May 24;102(21):7748-53 PMID: 15894619
Article Info
Journal
Nature genetics
Abbr.
Nat Genet
ISSN
1546-1718
Published
2017-00-00
Epub
2016-00-05
Pages
162-168
Language
English
Region
United States
NLM ID
9216904
Subset
IM
Analysis Services
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