A quantitative genetic basis for leaf morphology in a set of precisely defined tomato introgression lines

Plant Cell

Volumn 25, Issue 7, 2013, Pages 2465-2481

  Chitwood, Daniel H ^a   Kumar, Ravi ^a   Headland, Lauren R ^a   Ranjan, Aashish ^a   Covington, Michael F ^a   Ichihashi, Yasunori ^a   Fulop, Daniel ^a   Jiménez Gómez, José M ^a,b   Peng, Jie ^a   Maloof, Julin N ^a   Sinhaa, Neelima R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LYCOPERSICON ESCULENTUM; LYCOPERSICON PENNELLII;

VEGETABLE PROTEIN;

ARTICLE; CHROMOSOME MAP; FRUIT; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; METABOLISM; PHENOTYPE; PLANT GENE; PLANT GENOME; PLANT LEAF; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT LOCUS; SOLANUM; SPECIES DIFFERENCE; TOMATO;

CHROMOSOME MAPPING; FRUIT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME, PLANT; GENOTYPE; LYCOPERSICON ESCULENTUM; PHENOTYPE; PLANT LEAVES; PLANT PROTEINS; PRINCIPAL COMPONENT ANALYSIS; QUANTITATIVE TRAIT LOCI; SOLANUM; SPECIES SPECIFICITY;

EID: 84883165895     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.112391     Document Type: Article

References (93)

1. Abramoff, M.D., Magelhaes, P.J., and Ram, S.J. (2004). Image processing with ImageJ. Biophotonics International 11: 36-42.
2. Bailey, I.W., and Sinnott, E.W. (1915). A botanical index of Cretaceous and Tertiary climates. Science 41: 831-834.
3. Barkoulas, M., Galinha, C., Grigg, S.P., and Tsiantis, M. (2007). From genes to shape: Regulatory interactions in leaf development. Curr. Opin. Plant Biol. 10: 660-666.
4. Baxter, C.J., Carrari, F., Bauke, A., Overy, S., Hill, S.A., Quick, P.W., Fernie, A.R., and Sweetlove, L.J. (2005). Fruit carbohydrate metabolism in an introgression line of tomato with increased fruit soluble solids. Plant Cell Physiol. 46: 425-437.
5. Benjamini, Y., and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57: 289-300.
6. Canady, M.A., Meglic, V., and Chetelat, R.T. (2005). A library of Solanum lycopersicoides introgression lines in cultivated tomato. Genome 48: 685-697.
7. Carmel-Goren, L., Liu, Y.S., Lifschitz, E., and Zamir, D. (2003). The SELF-PRUNING gene family in tomato. Plant Mol. Biol. 52: 1215-1222.
8. Chitwood, D.H., Headland, L.R., Filiault, D.L., Kumar, R., Jiménez-Gómez, J.M., Schrager, A.V., Park, D.S., Peng, J., Sinha, N.R., and Maloof, J.N. (2012a). Native environment modulates leaf size and response to simulated foliar shade across wild tomato species. PLoS ONE 7: e29570.
9. Chitwood, D.H., Headland, L.R., Kumar, R., Peng, J., Maloof, J.N., and Sinha, N.R. (2012b). The developmental trajectory of leaflet morphology in wild tomato species. Plant Physiol. 158: 1230-1240.
10. Chitwood, D.H., Headland, L.R., Ranjan, A., Martinez, C.C., Braybrook, S.A., Koenig, D.P., Kuhlemeier, C., Smith, R.S., and Sinha, N.R. (2012c). Leaf asymmetry as a developmental constraint imposed by auxin-dependent phyllotactic patterning. Plant Cell 24: 2318-2327.
11. Chitwood, D.H., Maloof, J.N., and Sinha, N.R. (2013). Dynamic transcriptomic profiles between tomato and a wild relative reflect distinct developmental architectures. Plant Physiol. 162: 537-552.
12. Chitwood, D.H., Naylor, D.T., Thammapichai, P., Weeger, A.C.S., Headland, L.R., and Sinha, N.R. (2012d). Conflict between intrinsic leaf asymmetry and phyllotaxis in the resupinate leaves of Alstroemeria psittacina. Front. Plant Sci. 3: 182.
13. Chitwood, D.H., and Sinha, N.R. (2013). A census of cells in time: Quantitative genetics meets developmental biology. Curr. Opin. Plant Biol. 16: 92-99.
14. Cnops, G., Jover-Gil, S., Peters, J.L., Neyt, P., De Block, S., Robles, P., Ponce, M.R., Gerats, T., Micol, J.L., and Van Lijsebettens, M. (2004). The rotunda2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis. J. Exp. Bot. 55: 1529-1539.
15. Cong, B., Barrero, L.S., and Tanksley, S.D. (2008). Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication. Nat. Genet. 40: 800-804.
16. Do, P.T., Prudent, M., Sulpice, R., Causse, M., and Fernie, A.R. (2010). The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiol. 154: 1128-1142.
17. Duvick, D.N. (2005). Genetic progress in yield of United States maize (Zea mays L.). Maydica 50: 193-202.
18. Eshed, Y., Izhaki, A., Baum, S.F., Floyd, S.K., and Bowman, J.L. (2004). Asymmetric leaf development and blade expansion in are mediated by KANADI and YABBY activities. Development 131: 2997-3006.
19. Eshed, Y., and Zamir, D. (1995). An introgression line population of Lycopersicon pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141: 1147-1162.
20. Frary, A., Fritz, L.A., and Tanksley, S.D. (2004). A comparative study of the genetic bases of natural variation in tomato leaf, sepal, and petal morphology. Theor. Appl. Genet. 109: 523-533.
21. Frary, A., Nesbitt, T.C., Grandillo, S., Knaap, E., Cong, B., Liu, J., Meller, J., Elber, R., Alpert, K.B., and Tanksley, S.D. (2000). fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 289: 85-88.
22. Fridman, E., Carrari, F., Liu, Y.S., Fernie, A.R., and Zamir, D. (2004). Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305: 1786-1789.
23. Geigenberger, P., Regierer, B., Lytovchenko, A., Leisse, A., Schauer, N., Springer, F., Kossmann, J., and Fernie, A.R. (2004). Heterologous expression of a ketohexokinase in potato plants leads to inhibited rates of photosynthesis, severe growth retardation and abnormal leaf development. Planta 218: 569-578.
24. Givnish, T.J., and Vermeij, G.J. (1976). Sizes and shapes of liane leaves. Am. Nat. 110: 743-778.
25. Goff, S.A., et al. (2011). The iPlant Collaborative: Cyberinfrastructure for plant biology. Front. Plant Sci. 2: 34.
26. Golz, J.F., Roccaro, M., Kuzoff, R., and Hudson, A. (2004). GRAMINIFOLIA promotes growth and polarity of Antirrhinum leaves. Development 131: 3661-3670.
27. Greenwood, D.R. (1992). Taphonomic constraints on foliar physiognomic interpretations of Late Cretaceous and Tertiary palaeoclimates. Rev. Palaeobot. Palynol. 71: 149-190.
28. Hackel, A., Schauer, N., Carrari, F., Fernie, A.R., Grimm, B., and Kühn, C. (2006). Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J. 45: 180-192.
29. Heatherington, S.E., Smillie, R.M., and Davies, W.J. (1998). Photosynthetic activites of vegetative and fruiting tissues of tomato. J. Exp. Bot. 49: 1173-1181.
30. Heichel, G.H., and Anagnostakis, S.L. (1978). Stomatal response to light of Solanum pennellii, Lycopersicon esculentum, and a graftinduced chimera. Plant Physiol. 62: 387-390.
31. Holtan, H.E.E., and Hake, S. (2003). Quantitative trait locus analysis of leaf dissection in tomato using Lycopersicon pennellii segmental introgression lines. Genetics 165: 1541-1550.
32. Iwata, H., Niikura, S., Matsuura, S., Takano, Y., and Ukai, Y. (1998). Evaluation of variation of root shape of Japanese radish (Raphanus sativus L.) based on image analysis using elliptic Fourier descriptors. J. Hered. 93: 384-385.
33. Iwata, H., and Ukai, Y. (2002). SHAPE: A computer program package for quantitative evaluation of biological shapes based on elliptic Fourier descriptors. J. Hered. 93: 384-385.
34. Jiang, C., Wright, R.J., Woo, S.S., DelMonte, T.A., and Paterson, A.H. (2000). QTL analysis of leaf morphology in tetraploid Gossypoium (cotton). Theor. Appl. Genet. 100: 409-418.
35. Jones, B., Frasse, P., Olmos, E., Zegzouti, H., Li, Z.G., Latché, A., Pech, J.C., and Bouzayen, M. (2002). Down-regulation of DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. Plant J. 32: 603-613.
36. Jones, C.M., Rick, C.M., Adams, D., Jernstedt, J., and Chetelat, R.T. (2007). 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. 94: 935-947.
37. Kerstetter, R.A., Bollman, K., Taylor, R.A., Bomblies, K., and Poethig, R.S. (2001). KANADI regulates organ polarity in Arabidopsis. Nature 411: 706-709.
38. Kim, M., McCormick, S., Timmermans, M., and Sinha, N. (2003a). The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424: 438-443.
39. Kim, M., Pham, T., Hamidi, A., McCormick, S., Kuzoff, R.K., and Sinha, N. (2003b). Reduced leaf complexity in tomato wiry mutants suggests a role for PHAN and KNOX genes in generating compound leaves. Development 130: 4405-4415.
40. Kimura, S., Koenig, D., Kang, J., Yoong, F.Y., and Sinha, N. (2008). Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr. Biol. 18: 672-677.
41. Koboldt, D.C., Zhang, Q., Larson, D.E., Shen, D., McLellan, M.D., Lin, L., Miller, C.A., Mardis, E.R., Ding, L., andWilson, R.K. (2012). VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22: 568-576.
42. Koenig, D., et al. (2013). Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc. Natl. Acad. Sci. USA 110: E2655-E2662.
43. Krzywinski, M., Birol, I., Jones, S., and Marra, M. (2011). Hive plots-Rational approach to visualizing networks. Brief. Bioinform. doi: 10.1093/bib/bbr069.
44. Kumar, R., Ichihashi, Y., Kimura, S., Chitwood, D.H., Headland, L.R., Peng, J., Maloof, J.N., and Sinha, N.R. (2012). A highthroughput method for Illumina RNA-Seq library preparation. Front. Plant Sci. 3: 202.
45. Langlade, N.B., Feng, X., Dransfield, T., Copsey, L., Hanna, A.I., Thébaud, C., Bangham, A., Hudson, A., and Coen, E. (2005). Evolution through genetically controlled allometry space. Proc. Natl. Acad. Sci. USA 102: 10221-10226.
46. Lawson, T., Bryant, B., Lefebvre, S., Lloyd, J.C., and Raines, C.A. (2006). Decreased SBPase activity alters growth and development in transgenic tobacco plants. Plant Cell Environ. 29: 48-58.
47. Li, H., and Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
48. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., and Durbin, R.1000 Genome Project Data Processing Subgroup (2009). The sequence alignment/map format and SAM tools. Bioinformatics 25: 2078-2079.
49. Li, W., and Chetelat, R.T. (2010). A pollen factor linking inter-and intraspecific pollen rejection in tomato. Science 330: 1827-1830.
50. Liu, Y.-S., and Zamir, D. (1999). Second generation L. pennellii introgression lines and the concept of bin mapping. Report of the Tomato Genetics Cooperative 49: 26-30.
51. Liu, Z., Jia, L., Wang, H., and He, Y. (2011). HYL1 regulates the balance between adaxial and abaxial identity for leaf flattening via miRNA-mediated pathways. J. Exp. Bot. 62: 4367-4381.
52. Lytovchenko, A., et al. (2011). Tomato fruit photosynthesis is seemingly unimportant in primary metabolism and ripening but plays a considerable role in seed development. Plant Physiol. 157: 1650-1663.
53. Massonnet, C., Tisné, S., Radziejwoski, A., Vile, D., De Veylder, L., Dauzat, M., and Granier, C. (2011). New insights into the control of endoreduplication: endoreduplication could be driven by organ growth in Arabidopsis leaves. Plant Physiol. 157: 2044-2055.
54. Monforte, A.J., and Tanksley, S.D. (2000). Development of a set of near isogenic and backcross recombinant inbred lines containing most of the Lycopersicon hirsutum genome in a L. esculentum genetic background: a tool for gene mapping and gene discovery. Genome 43: 803-813.
55. Monson-Miller, J., Sanchez-Mendez, D.C., Fass, J., Henry, I.M., Tai, T.H., and Comai, L. (2012). Reference genome-independent assessment of mutation density using restriction enzyme-phased sequencing. BMC Genomics 13: 72.
56. Moyle, L.C. (2008). Ecological and evolutionary genomics in the wild tomatoes (Solanum sect. Lycopersicon). Evolution 62: 2995-3013.
57. Nicotra, A.B., Leigh, A., Boyce, C.K., Jones, C.S., Niklas, K.J., Royer, D.L., and Tsukaya, H. (2011). The evolution and functional significance of leaf shape in the angiosperms. Funct. Plant Biol. 38: 535-552.
58. Parkhurst, D.F., and Loucks, O.L. (1972). Optimal leaf size in relation to environment. J. Ecol. 60: 505-537.
59. Pérez-Pérez, J.M., Serrano-Cartagena, J., and Micol, J.L. (2002). Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162: 893-915.
60. Poorter, H., Niinemets, U., Walter, A., Fiorani, F., and Schurr, U. (2010). A method to construct dose-response curves for a wide range of environmental factors and plant traits by means of a metaanalysis of phenotypic data. J. Exp. Bot. 61: 2043-2055.
61. Powell, A.L.T., et al. (2012). Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336: 1711-1715.
62. R Development Core Team (2011). R: A Language and Environment for Statistical Computing. (Vienna, Austria: R Foundation for Statistical Computing).
63. Raines, C.A., and Paul, M.J. (2006). Products of leaf primary carbon metabolism modulate the developmental programme determining plant morphology. J. Exp. Bot. 57: 1857-1862.
64. Ranjan, A., Ichihashi, Y., and Sinha, N.R. (2012). The tomato genome: Implications for plant breeding, genomics and evolution. Genome Biol. 13: 167.
65. Robinson, M.D., and Oshlack, A. (2010). A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11: R25.
66. Rousseaux, M.C., Jones, C.M., Adams, D., Chetelat, R., Bennett, A., and Powell, A. (2005). QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor. Appl. Genet. 111: 1396-1408.
67. Sagar, M., et al. (2013). SlARF4, an auxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol. 161: 1362-1374.
68. Schauer, N., Semel, Y., Balbo, I., Steinfath, M., Repsilber, D., Selbig, J., Pleban, T., Zamir, D., and Fernie, A.R. (2008). Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20: 509-523.
69. Schauer, N., et al. (2006). Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat. Biotechnol. 24: 447-454.
70. Semel, Y., Nissenbaum, J., Menda, N., Zinder, M., Krieger, U., Issman, N., Pleban, T., Lippman, Z., Gur, A., and Zamir, D. (2006). Overdominant quantitative trait loci for yield and fitness in tomato. Proc. Natl. Acad. Sci. USA 103: 12981-12986.
71. Seymour, D.K., Filiault, D.L., Henry, I.M., Monson-Miller, J., Ravi, M., Pang, A., Comai, L., Chan, S.W., and Maloof, J.N. (2012). Rapid creation of Arabidopsis doubled haploid lines for quantitative trait locus mapping. Proc. Natl. Acad. Sci. USA 109: 4227-4232.
72. Siegfried, K.R., Eshed, Y., Baum, S.F., Otsuga, D., Drews, G.N., and Bowman, J.L. (1999). Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126: 4117-4128.
73. Stahle, M.I., Kuehlich, J., Staron, L., von Arnim, A.G., and Golz, J.F. (2009). YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21: 3105-3118.
74. Steindler, C., Matteucci, A., Sessa, G., Weimar, T., Ohgishi, M., Aoyama, T., Morelli, G., and Ruberti, I. (1999). Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. Development 126: 4235-4245.
75. Steinhauser, M.C., Steinhauser, D., Gibon, Y., Bolger, M., Arrivault, S., Usadel, B., Zamir, D., Fernie, A.R., and Stitt, M. (2011). Identification of enzyme activity quantitative trait loci in a Solanum lycopersicum x Solanum pennellii introgression line population. Plant Physiol. 157: 998-1014.
76. Sterken, R., Kiekens, R., Boruc, J., Zhang, F., Vercauteren, A., Vercauteren, I., De Smet, L., Dhondt, S., Inzé, D., De Veylder, L., Russinova, E., and Vuylsteke, M. (2012). Combined linkage and association mapping reveals CYCD5;1 as a quantitative trait gene for endoreduplication in Arabidopsis. Proc. Natl. Acad. Sci. USA 109: 4678-4683.
77. Stevens, M.A., and Rick, C.M. (1986). Genetics and breeding. In The Tomato Crop, J.G. Atherton and J. Rudich, eds (London, New York: Chapman and Hall), pp. 36-109.
78. Stevens, R., Buret, M., Duffé, P., Garchery, C., Baldet, P., Rothan, C., and Causse, M. (2007). Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol. 143: 1943-1953.
79. Tian, F., Bradbury, P.J., Brown, P.J., Hung, H., Sun, Q., Flint-Garcia, S., Rocheford, T.R., McMullen, M.D., Holland, J.B., and Buckler, E.S. (2011). Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat. Genet. 43: 159-162.
80. Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635-641.
81. Toubiana, D., Semel, Y., Tohge, T., Beleggia, R., Cattivelli, L., Rosental, L., Nikoloski, Z., Zamir, D., Fernie, A.R., and Fait, A. (2012). Metabolic profiling of a mapping population exposes new insights in the regulation of seed metabolism and seed, fruit, and plant relations. PLoS Genet. 8: e1002612.
82. Trapnell, C., Pachter, L., and Salzberg, S.L. (2009). TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105-1111.
83. Tsai, C.H., Miller, A., Spalding, M., and Rodermel, S. (1997). Source strength regulates an early phase transition of tobacco shoot morphogenesis. Plant Physiol. 115: 907-914.
84. Wickham, H. (2009). ggplot2: Elegant Graphics for Data Analysis. (New York: Springer).
85. Wilf, P., Wing, S.L., Greenwood, D.R., and Greenwood, C.L. (1998). Using fossil leaves as paleoprecipitation indicators: An Eocene example. Geology 26: 203-206.
86. Willmann, M.R., and Poethig, R.S. (2011). The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis. Development 138: 677-685.
87. Wolfe, J.A. (1971). Tertiary climatic fluctuations and methods of analysis of tertiary floras. Palaeogeogr. Palaeoclimatol. Palaeoecol. 9: 27-57.
88. Wu, S., Xiao, H., Cabrera, A., Meulia, T., and van der Knaap, E. (2011). SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol. 157: 1175-1186.
89. Xiao, H., Jiang, N., Schaffner, E., Stockinger, E.J., and van der Knaap, E. (2008). A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit. Science 319: 1527-1530.
90. Yifhar, T., Pekker, I., Peled, D., Friedlander, G., Pistunov, A., Sabban, M., Wachsman, G., Alvarez, J.P., Amsellem, Z., and Eshed, Y. (2012). Failure of the tomato trans-acting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24: 3575-3589.
91. Young, M.D., Wakefield, M.J., Smyth, G.K., and Oshlack, A. (2010). Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biol. 11: R14.
92. Zamir, D. (2013). Where have all the crop phenotypes gone? PLoS Biol. 11: e1001595.
93. Zanor, M.I., Rambla, J.L., Chaïb, J., Steppa, A., Medina, A., Granell, A., Fernie, A.R., and Causse, M. (2009). Metabolic characterization of loci affecting sensory attributes in tomato allows an assessment of the influence of the levels of primary metabolites and volatile organic contents. J. Exp. Bot. 60: 2139-2154.