Tomato Yield Heterosis Is Triggered by a Dosage Sensitivity of the Florigen Pathway That Fine-Tunes Shoot Architecture

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The superiority of hybrids has long been exploited in agriculture, and although many models explaining “heterosis” have been put forth, direct empirical support is limited. Particularly elusive have been cases of heterozygosity for single gene mutations causing heterosis under a genetic model known as overdominance. In tomato (Solanum lycopersicum), plants carrying mutations in SINGLE FLOWER TRUSS (SFT) encoding the flowering hormone florigen are severely delayed in flowering, become extremely large, and produce few flowers and fruits, but when heterozygous, yields are dramatically increased. Curiously, this overdominance is evident only in the background of “determinate” plants, in which the continuous production of side shoots and inflorescences gradually halts due to a defect in the flowering repressor SELF PRUNING (SP). How sp facilitates sft overdominance is unclear, but is thought to relate to the opposing functions these genes have on flowering time and shoot architecture. We show that sft mutant heterozygosity (sft/+) causes weak semi-dominant delays in flowering of both primary and side shoots. Using transcriptome sequencing of shoot meristems, we demonstrate that this delay begins before seedling meristems become reproductive, followed by delays in subsequent side shoot meristems that, in turn, postpone the arrest of shoot and inflorescence production. Reducing SFT levels in sp plants by artificial microRNAs recapitulates the dose-dependent modification of shoot and inflorescence production of sft/+ heterozygotes, confirming that fine-tuning levels of functional SFT transcripts provides a foundation for higher yields. Finally, we show that although flowering delays by florigen mutant heterozygosity are conserved in Arabidopsis, increased yield is not, likely because cyclical flowering is absent. We suggest sft heterozygosity triggers a yield improvement by optimizing plant architecture via its dosage response in the florigen pathway. Exploiting dosage sensitivity of florigen and its family members therefore provides a path to enhance productivity in other crops, but species-specific tuning will be required.

Vyšlo v časopise: Tomato Yield Heterosis Is Triggered by a Dosage Sensitivity of the Florigen Pathway That Fine-Tunes Shoot Architecture. PLoS Genet 9(12): e32767. doi:10.1371/journal.pgen.1004043
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004043

Souhrn

Zdroje

1. Darwin C (1868) The Variation of Animals and Plants under Domestication. 2.

2. CharlesworthD, WillisJH (2009) The genetics of inbreeding depression. Nat Rev Genet 10 : 783–796.

3. ShullGH (1908) The composition of a field of maize. Am Breed Assn Rep 4 : 269–301.

4. CrowJF (1948) Alternative Hypotheses of Hybrid Vigor. Genetics 33 : 477–487.

5. HochholdingerF, HoeckerN (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12 : 427–432.

6. LippmanZB, ZamirD (2007) Heterosis: revisiting the magic. Trends Genet 23 : 60–66.

7. SpringerNM, StuparRM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17 : 264–275.

8. ChenZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14 : 471–482.

9. SchnablePS, SpringerNM (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64 : 71–88.

10. BirchlerJA, YaoH, ChudalayandiS, VaimanD, VeitiaRA (2010) Heterosis. The Plant cell 22 : 2105–2112.

11. McMullenMD, KresovichS, VilledaHS, BradburyP, LiH, et al. (2009) Genetic properties of the maize nested association mapping population. Science 325 : 737–740.

12. StuberCW, LincolnSE, WolffDW, HelentjarisT, LanderES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132 : 823–839.

13. LiZK, LuoLJ, MeiHW, WangDL, ShuQY, et al. (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158 : 1737–1753.

14. LuoLJ, LiZK, MeiHW, ShuQY, TabienR, et al. (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genetics 158 : 1755–1771.

15. StuparRM, SpringerNM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173 : 2199–2210.

16. IshikawaA (2009) Mapping an overdominant quantitative trait locus for heterosis of body weight in mice. J Hered 100 : 501–504.

17. SchulerJF (1954) Natural Mutations in Inbred Lines of Maize and Their Heterotic Effect. I. Comparison of Parent, Mutant and Their F(1) Hybrid in a Highly Inbred Background. Genetics 39 : 908–922.

18. MukaiT, BurdickAB (1959) Single Gene Heterosis Associated with a Second Chromosome Recessive Lethal in Drosophila Melanogaster. Genetics 44 : 211–232.

19. RedeiGP (1962) Single Locus Heterosis. Zeitschrift Fur Vererbungslehre 93 : 164–&.

20. EfronY (1973) Specific differences in maize alcohol dehydrogenase: possible explanation of heterosis at the molecular level. Nat New Biol 241 : 41–42.

21. HallJG, WillsC (1987) Conditional overdominance at an alcohol dehydrogenase locus in yeast. Genetics 117 : 421–427.

22. GrobetL, MartinLJ, PonceletD, PirottinD, BrouwersB, et al. (1997) A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17 : 71–74.

23. MosherDS, QuignonP, BustamanteCD, SutterNB, MellershCS, et al. (2007) A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 3: e79.

24. DelneriD, HoyleDC, GkargkasK, CrossEJ, RashB, et al. (2008) Identification and characterization of high-flux-control genes of yeast through competition analyses in continuous cultures. Nat Genet 40 : 113–117.

25. KriegerU, LippmanZB, ZamirD (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42 : 459–463.

26. PnueliL, Carmel-GorenL, HarevenD, GutfingerT, AlvarezJ, et al. (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 : 1979–1989.

27. LifschitzE, EviatarT, RozmanA, ShalitA, GoldshmidtA, et al. (2006) 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 103 : 6398–6403.

28. Saltveit ME (2005) Post harvest biology and handling. In: Heuvelink E, editor. Tomatoes. Wallingford, U.K.: CABI Publishing. pp. 305–325.

29. Peet MM, Welles G (2005) Greenhouse tomato production. In: Heuvelink E, editor. Tomatoes. Wallingford, U.K.: CABI Publishing. pp. 257–304.

30. LippmanZB, CohenO, AlvarezJP, Abu-AbiedM, PekkerI, et al. (2008) The making of a compound inflorescence in tomato and related nightshades. PLoS Biol 6: e288.

31. EfroniI, BlumE, GoldshmidtA, EshedY (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. Plant Cell 20 : 2293–2306.

32. Swanson-WagnerRA, JiaY, DeCookR, BorsukLA, NettletonD, et al. (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci U S A 103 : 6805–6810.

33. JaegerKE, PullenN, LamzinS, MorrisRJ, WiggePA (2013) Interlocking feedback loops govern the dynamic behavior of the floral transition in Arabidopsis. Plant Cell 25 : 820–833.

34. ParkSJ, JiangK, SchatzMC, LippmanZB (2012) Rate of meristem maturation determines inflorescence architecture in tomato. Proc Natl Acad Sci U S A 109 : 639–644.

35. AlvarezJP, PekkerI, GoldshmidtA, BlumE, AmsellemZ, et al. (2006) Endogenous and synthetic microRNAs stimulate simultaneous, efficient, and localized regulation of multiple targets in diverse species. Plant Cell 18 : 1134–1151.

36. SchwabR, OssowskiS, RiesterM, WarthmannN, WeigelD (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell 18 : 1121–1133.

37. WiggePA (2011) FT, a mobile developmental signal in plants. Curr Biol 21: R374–378.

38. ShalitA, RozmanA, GoldshmidtA, AlvarezJP, BowmanJL, et al. (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci U S A 106 : 8392–8397.

39. KoornneefM, HanhartCJ, van der VeenJH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Molecular & general genetics : MGG 229 : 57–66.

40. ShannonS, Meeks-WagnerDR (1991) A Mutation in the Arabidopsis TFL1 Gene Affects Inflorescence Meristem Development. The Plant cell 3 : 877–892.

41. GoffSA (2011) A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol 189 : 923–937.

42. DoebleyJF, GautBS, SmithBD (2006) The molecular genetics of crop domestication. Cell 127 : 1309–1321.

43. IzawaT, TakahashiY, YanoM (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Current opinion in plant biology 6 : 113–120.

44. ZhaoK, TungCW, EizengaGC, WrightMH, AliML, et al. (2011) Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nature communications 2 : 467.

45. TsujiH, TaokaK, ShimamotoK (2011) Regulation of flowering in rice: two florigen genes, a complex gene network, and natural variation. Current opinion in plant biology 14 : 45–52.

46. BucklerES, HollandJB, BradburyPJ, AcharyaCB, BrownPJ, et al. (2009) The genetic architecture of maize flowering time. Science 325 : 714–718.

47. TanksleySD (2004) The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. The Plant cell 16 Suppl S181–189.

48. CongB, BarreroLS, TanksleySD (2008) Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nature genetics 40 : 800–804.

49. DoganlarS, FraryA, KuHM, TanksleySD (2002) Mapping quantitative trait loci in inbred backcross lines of Lycopersicon pimpinellifolium (LA1589). Genome/National Research Council Canada = Genome/Conseil national de recherches Canada 45 : 1189–1202.

50. GrandilloS, TanksleySD (1996) QTL analysis of horticultural traits differentiating the cultivated tomato from the closely related species Lycopersicon pimpinellifolium. Theoretical and Applied Genetics 92 : 935–951.

51. Jimenez-GomezJM, Alonso-BlancoC, BorjaA, AnastasioG, AngostoT, et al. (2007) Quantitative genetic analysis of flowering time in tomato. Genome/National Research Council Canada = Genome/Conseil national de recherches Canada 50 : 303–315.

52. PeraltaIE, SpoonerDM (2005) Morphological characterization and relationships of wild tomatoes (Solanum L. Section Lycopersicon). Monogr Syst Bot Missouri Bot Gard 227–257.

53. Flint-GarciaSA, BucklerES, TiffinP, ErsozE, SpringerNM (2009) Heterosis is prevalent for multiple traits in diverse maize germplasm. PLoS One 4: e7433.

54. SemelY, NissenbaumJ, MendaN, ZinderM, KriegerU, et al. (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proceedings of the National Academy of Sciences of the United States of America 103 : 12981–12986.

55. SchuelkeM, WagnerKR, StolzLE, HubnerC, RiebelT, et al. (2004) Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350 : 2682–2688.

56. JiangW, ZhouH, BiH, FrommM, YangB, et al. (2013) Demonstration of CRISPR/Cas9/sgRNA-mediated targeted gene modification in Arabidopsis, tobacco, sorghum and rice. Nucleic acids research 41 (20) e188 doi: 10.1093/nar/gkt780

57. ShanQ, WangY, LiJ, ZhangY, ChenK, et al. (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nature biotechnology 31 : 686–688.

58. TaokaK, OhkiI, TsujiH, KojimaC, ShimamotoK (2013) Structure and function of florigen and the receptor complex. Trends in plant science 18 : 287–294.

59. LifschitzE, EshedY (2006) Universal florigenic signals triggered by FT homologues regulate growth and flowering cycles in perennial day-neutral tomato. Journal of experimental botany 57 : 3405–3414.

60. MengX, MuszynskiMG, DanilevskayaON (2011) The FT-like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize. Plant Cell 23 : 942–960.

61. BlackmanBK, StrasburgJL, RaduskiAR, MichaelsSD, RiesebergLH (2010) The role of recently derived FT paralogs in sunflower domestication. Curr Biol 20 : 629–635.

62. QuinbyJR, KarperRE (1946) Heterosis in sorghum resulting from the heterozygous condition of a single gene that affects duration of growth. Am J Bot 33 : 716–721.

63. ComadranJ, KilianB, RussellJ, RamsayL, SteinN, et al. (2012) Natural variation in a homolog of Antirrhinum CENTRORADIALIS contributed to spring growth habit and environmental adaptation in cultivated barley. Nat Genet 44 : 1388–1392.

64. PinPA, BenllochR, BonnetD, Wremerth-WeichE, KraftT, et al. (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330 : 1397–1400.

65. KwakM, VelascoD, GeptsP (2008) Mapping homologous sequences for determinacy and photoperiod sensitivity in common bean (Phaseolus vulgaris). J Hered 99 : 283–291.

66. RepinskiSL, KwakM, GeptsP (2012) The common bean growth habit gene PvTFL1y is a functional homolog of Arabidopsis TFL1. Theor Appl Genet 124 : 1539–1547.

67. FernandezL, TorregrosaL, SeguraV, BouquetA, Martinez-ZapaterJM (2010) Transposon-induced gene activation as a mechanism generating cluster shape somatic variation in grapevine. Plant J 61 : 545–557.

68. NavarroC, AbelendaJA, Cruz-OroE, CuellarCA, TamakiS, et al. (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478 : 119–122.

69. IwataH, GastonA, RemayA, ThouroudeT, JeauffreJ, et al. (2012) The TFL1 homologue KSN is a regulator of continuous flowering in rose and strawberry. Plant J 69 : 116–125.

70. TianZ, WangX, LeeR, LiY, SpechtJE, et al. (2010) Artificial selection for determinate growth habit in soybean. Proc Natl Acad Sci U S A 107 : 8563–8568.

71. LiuB, WatanabeS, UchiyamaT, KongF, KanazawaA, et al. (2010) The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1. Plant Physiol 153 : 198–210.

72. HarigL, BeineckeFA, OltmannsJ, MuthJ, MullerO, et al. (2012) Proteins from the FLOWERING LOCUS T-like subclade of the PEBP family act antagonistically to regulate floral initiation in tobacco. Plant J doi: []10.1111/j.1365-313X.2012.05125.x [Epub ahead of print].

73. HeddenP (2003) The genes of the Green Revolution. Trends in genetics : TIG 19 : 5–9.

74. MendaN, SemelY, PeledD, EshedY, ZamirD (2004) In silico screening of a saturated mutation library of tomato. The Plant journal : for cell and molecular biology 38 : 861–872.

75. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.

76. Tomato GenomeC (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485 : 635–641.

77. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25 : 2078–2079.

78. RDC T (2011) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

79. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26 : 139–140.

80. AllenE, HowellMD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Seminars in cell & developmental biology 21 : 798–804.

81. MoissiardG, ParizottoEA, HimberC, VoinnetO (2007) Transitivity in Arabidopsis can be primed, requires the redundant action of the antiviral Dicer-like 4 and Dicer-like 2, and is compromised by viral-encoded suppressor proteins. RNA 13 : 1268–1278.