Crop management impacts the efficiency of quantitative trait loci (QTL) detection and use: Case study of fruit load×QTL interactions

Journal of Experimental Botany

Volumn 65, Issue 1, 2014, Pages 11-22

  Kromdijk, J ^a   Bertin, N ^b   Heuvelink, E ^a   Molenaar, J ^a,c   De Visser, P H B ^a   Marcelis, L F M ^a   Struik, P C ^a,d  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Domaine Saint Paul   (France)

^c Netherlands Consortium for Systems Biology   (Netherlands)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Breeding; environment interaction; environment interactions; fruit load; fruit quality; gene expression; genotype ; QTL

Indexed keywords

BIOLOGICAL MODEL; BREEDING; CHROMOSOME MAP; CROP; ENVIRONMENT INTERACTION.; ENVIRONMENT INTERACTIONS; FRUIT; FRUIT LOAD; FRUIT QUALITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE×; PHENOTYPE; PHYSIOLOGY; QTL×; QUANTITATIVE TRAIT LOCUS; REVIEW;

BREEDING; ENVIRONMENT INTERACTION.; ENVIRONMENT INTERACTIONS; FRUIT LOAD; FRUIT QUALITY; GENE EXPRESSION; GENOTYPE×; QTL×;

BREEDING; CHROMOSOME MAPPING; CROPS, AGRICULTURAL; FRUIT; GENE EXPRESSION REGULATION, PLANT; GENE-ENVIRONMENT INTERACTION; GENOTYPE; MODELS, GENETIC; PHENOTYPE; QUANTITATIVE TRAIT LOCI;

EID: 84892747822     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ert365     Document Type: Review

References (102)

1. Ainsworth EA, Bush DR. 2011. Carbohydrate export from the leaf: a highly regulated process and target to enhance photosynthesis and productivity. Plant Physiology 155, 64-69.
2. Baldazzi V, Bertin N, De Jong H, Génard M. 2012. Towards multiscale plant models: integrating cellular networks. Trends in Plant Science 17, 728-736.
3. Baldet P, Hernould M, Laporte F, Mounet F, Just D, Mouras A, Chevalier C, Rothan C. 2006. The expression of cell proliferation-related genes in early developing fowers is affected by a fruit load reduction in tomato plants. Journal of Experimental Botany 57, 961-970.
4. Bangerth KF. 2009. Floral induction in mature, perennial angiosperm fruit trees: similarities and discrepancies with annual/biennial plants and the involvement of plant hormones, Scientia Horticulturae 122, 153-163.
5. Bertin N. 1995. Competition for assimilates and fruit position affect fruit set in indeterminate greenhouse tomato. Annals of Botany 75, 55-65.
6. Bertin N. 2005. Analysis of the tomato fruit growth response to temperature and plant fruit load in relation to cell division, cell expansion and DNA endoreduplication. Annals of Botany 95, 439-447.
7. Bertin N, Borel C, Brunel B, Cheniclet C, Causse M. 2003. Do genetic make-up and growth manipulation affect tomato fruit size by cell number, or cell size and DNA endoreduplication? Annals of Botany 92, 415-424.
8. Bertin N, Causse M, Brunel B, Tricon D, Génard M. 2009. Identifcation of growth processes involved in QTLs for tomato fruit size and composition. Journal of Experimental Botany 60, 237-248.
9. Bertin N, Gautier H, Roche C. 2002. Number of cells in tomato fruit depending on fruit position and source-sink balance during plant development. Plant Growth Regulation 36, 105-112.
10. Bertin N, Guichard S, Leonardi C, Longuenesse JJ, Langlois D, Navez B. 2000. Seasonal evolution of the quality of fresh glasshouse tomatoes under Mediterranean conditions, as affected by air vapour pressure defcit and plant fruit load. Annals of Botany 85, 741-750.
11. Bertin N, Martre P, Génard M, Quilot B, Salon C. 2010. Under what circumstances can process-based simulation models link genotype to phenotype for complex traits? Case-study of fruit and grain quality traits. Journal of Experimental Botany 61, 955-967.
12. Bihmidine S, Hunter CT III, Johns CE, Koch KE, Braun DM. 2013. Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Frontiers in Plant Science 4, 177.
13. Bohner J, Bangerth F. 1988. Effects of fruit set sequence and defoliation on cell number, cell size and hormone levels of tomato fruits (Lycopersicon esculentum Mill.) within a truss. Plant Growth Regulation 7, 141-155.
14. Bourdon M, Frangne N, Mathieu-Rivet E, Nafati M, Cheniclet C, Renaudin JP, Chevalier C. 2010. Endoreduplication and growth of feshy fruits. Progress in Botany 71, 101-132.
15. Boyd LM, Barnett AM. 2011. Manipulation of whole-vine carbon allocation using girdling, pruning, and fruit thinning affects fruit numbers and quality in kiwifruit. HortScience 46, 590-595.
16. Breia R, Vieira S, Marques da Silva J, Gerós H, Cunha A. 2013. Mapping grape berry photosynthesis by chlorophyll fuorescence imaging: The effect of saturating pulse intensity in different tissues. Photochemistry and Photobiology 89, 579-585.
17. Bünger-Kibler S, Bangerth F. 1983. Relationship between cell number, cell size and fruit size of seeded fruits of tomato (Lycopersicon esculentum Mill.), and those induced parthenocarpically by the application of plant growth regulators. Plant Growth Regulation 1, 143-154.
18. Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP. 2005. Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth. Plant Physiology 139, 1984-1994.
19. Chevalier C, Nafati M, Mathieu-Rivet E, Bourdon M, Frangne N, Cheniclet C, Renaudin JP, Gévaudant F, Hernould M. 2011. Elucidating the functional role of endoreduplication in tomato fruit development. Annals of Botany 107, 1159-1169.
20. Dai ZW, Ollat N, Gomès E, et al. 2011. Ecophysiological, genetic, and molecular causes of variation in grape berry weight and composition: a review. American Journal of Enology and Viticulture 62, 413-425.
21. Dai ZW, Vivin P, Robert T, Milin S, Li SH, Génard M. 2009. Model-based analysis of sugar accumulation in response to source-sink ratio and water supply in grape (Vitis vinifera) berries. Functional Plant Biology 36, 527-540.
22. Dal Cin V, Danesin M, Botton A, Boschetti A, Dorigoni A, Ramina A. 2007. Fruit load and elevation affect ethylene biosynthesis and action in apple fruit (Malus domestica L. Borkh) during development, maturation and ripening. Plant, Cell & Environment 30, 1480-1485.
23. Dash M, Johnson LK, Malladi A. 2013. Reduction of fruit load affects early fruit growth in apple by enhancing carbohydrate availability, altering the expression of cell production-related genes, and increasing cell producton. Journal of the American Society of Horticultural Science 138, 253-262.
24. Dash M, Malladi A. 2012. The AINTEGUMENTA genes, MdANT1 and MdANT2, are associated with the regulation of cell production during fruit growth in apple (Malus×domestica Borkh.). BMC Plant Biology 12, 98.
25. Devoghalaere F, Doucen T, Guitton B, et al. 2012. A genomics approach to understanding the role of auxin in apple (Malus×domestica) fruit size control. BMC Plant Biology 12, 7.
26. Do PT, Prudent M, Sulpice R, Causse M, Fernie AR. 2010. The infuence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiology 154, 1128-1142.
27. Fanasca S, Martino A, Heuvelink E, Stanghellini C. 2007. Effect of electrical conductivity, fruit pruning, and truss position on quality in greenhouse tomato fruit. Journal of Horticultural Science & Biotechnology 82, 488-494.
28. Fanwoua J, de Visser PHB, Heuvelink E, Angenent G, Yin X, Marcelis LFM, Struik PC. 2012. Histological and molecular investigation of the basis for variation in tomato fruit size in response to fruit load and genotype. Functional Plant Biology 39, 754-763.
29. Fanwoua J, de Visser PHB, Heuvelink E, Yin X, Struik PC, Marcelis LFM. 2013. A dynamic model of tomato fruit growth integrating cell division, cell growth and endoreduplication. Functional Plant Biology 40, 1098-1114. http://dx.doi.org/10.1071/FP13007.
30. Gautier H, Guichard S, Tchamitchian M. 2001. Modulation of competition between fruits and leaves by fower pruning and water fogging, and consequences on tomato leaf and fruit growth. Annals of Botany 88, 645-652
31. Gautier H, Rocci A, Buret M, Grasselly D, Causse M. 2005. Fruit load or fruit position alters response to temperature and subsequently cherry tomato quality. Journal of the Science of Food and Agriculture 85, 1009-1016.
32. Génard M, Gouble B. 2005. ETHY. A theory of fruit climacteric ethylene emission. Plant Physiology 139, 531-545.
33. Goffnet MC, Robinson TL, Lakso AN. 1995. A comparison of 'Empire' apple fruit size and anatomy in unthinned and hand-thinned trees. Journal of Horticultural Science 70, 375-387.
34. Guardiola JL, García-Luis A. 2000. Increasing fruit size in citrus. Thinning and stimulation of fruit growth. Plant Growth Regulation 31, 121-132.
35. Guichard S, Gary C, Leonardi C, Bertin N. 2005. Analysis of growth and water relations of tomato fruits in relation to air vapor pressure defcit and plant fruit load. Journal of Plant Growth Regulation 24, 201-213.
36. Hammer G, Cooper M, Tardieu F. Welch S, Walsh B, van Eeuwijk FA, Chapman S, Podlich D. 2006. Models for navigating biological complexity in breeding improved crop plants. Trends in Plant Science 11, 587-593.
37. Harada T, Kurahashi W, Yanai M, Wakasa Y, Satoh T. 2005. Involvement of cell proliferation and cell enlargement in increasing the fruit size of Malus species. Scientia Horticulturae 105, 447-456
38. Hartig K, Beck E. 2006. Crosstalk between auxin, cytokinins, and sugars in the plant cell cycle. Plant Biology 8, 389-396.
39. Higashi K, Hosoya K, Ezura H. 1999. Histological analysis of fruit development between two melon (Cucumis melo L. reticulatus) genotypes setting a different size of fruit. Journal of Experimental Botany 50, 1593-1597.
40. Hiratsuka S, Yokoyama Y, Nishimura H, Miyazaki, Nada K. 2012. Fruit photosynthesis and phosphoenolpyruvate carboxylase activity as affected by lightproof fruit bagging in Satsuma mandarin. Journal of the American Society of Horticultural Science 137, 215-220.
41. Houel C, Martin-Magniette ML, Nicolas SD, et al. 2013. Genetic variability of berry size in the grapevine (Vitis vinifera L.). Australian Journal of Grape and Wine Research 19, 208-220.
42. Iglesias DJ, Lliso I, Tadeo FR, Talon M. 2002. Regulation of photosynthesis through source: sink imbalance in citrus is mediated by carbohydrate content in leaves. Physiologia Plantarum 116, 563-572.
43. Iglesias DJ, Tadeo FR, Primo-Millo E, Talon M. 2003. Fruit set dependence on carbohydrate availability in citrus trees. Tree Physiology 23, 199-204.
44. Johnson LK, Malladi A, Scott NeSmith D. 2011. Differences in cell number facilitate fruit size variation in Rabbiteye blueberry genotypes. Journal of the American Society of Horticultural Science 136, 10-15.
45. Keurentjes JJB, Angenent GC, Dicke M, Martins Dos Santos VAP, Molenaar J, van der Putten WH, de Ruiter PC, Struik PC, Thomma BPHJ. 2011. Redefning plant systems biology: from cell to community. Trends in Plant Science 16, 183-190.
46. Keurentjes JJB, Molenaar J, Zwaan BJ. 2013. Predictive modelling of complex agronomic and biological systems. Plant, Cell & Environment 36, 1700-7110.
47. Kittikorn M, Okawa K, Ohara H, Kotoda N, Wada M, Yokoyama M, Ifuku O, Yoshida S, Kondo S. 2011. Effects of fruit load, shading, and 9, 10-ketol-octadecadienoic acid (KODA) application on MdTFL1 and MdFT1 genes in apple buds. Plant Growth Regulation 64, 75-81.
48. Koch K. 2004. Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235-246.
49. Léchaudel M, Génard M, Lescourret F, Urban L, Jannoyer M. 2005. Modeling effects of weather and source-sink relationships on mango fruit growth. Tree Physiology 25, 583-597.
50. Link H. 2000. Signifcance of fower and fruit thinning on fruit quality. Plant Growth Regulation 31, 17-26.
51. Lockhart JA. 1965. An analysis of irreversible plant cell elongation. Journal of Theoretical Biology 8, 264-275.
52. Lytovchenko A, Eickmeier I, Pons C, et al. 2011. Tomato fruit photosynthesis is seemingly unimportant in primary metabolism and ripening but plays a considerable role in seed development. Plant Physiology 157, 1650-1663.
53. Malladi A, Hirst PM. 2010. Increase in fruit size of a spontaneous mutant of 'Gala' apple (Malus×domestica Borkh.) is facilitated by altered cell production and enhanced cell size. Journal of Experimental Botany 61, 3003-3013.
54. Marcelis LFM. 1993. Effect of assimilate supply on the growth of individual cucumber fruits. Physiologia Plantarum 87, 313-320.
55. Marcelis LFM. 1996. Sink strength as a determinant of dry matter partitioning in the whole plant. Journal of Experimental Botany 47, 1281-1291.
56. Marcelis LFM, Baan Hofman-Eijer LR. 1995. The contribution of fruit photosynthesis to the carbon requirement of cucumber fruits as affected by irradiance, temperature and ontogeny. Physiologia Plantarum 93, 476-483.
57. Marcelis LFM, Heuvelink E, Baan Hofman-Eijer LR, den Bakker J, Xue LB. 2004. Flower and fruit abortion in sweet pepper in relation to source and sink strength. Journal of Experimental Botany 55, 2261-2268.
58. Massot C, Génard M, Stevens R, Gautier H. 2010. Fluctuations in sugar content are not determinant in explaining variations in vitamin C in tomato fruit. Plant Physiology and Biochemistry 48, 751-757.
59. Montes JM, Melchinger AE, Reif JC. 2007. Novel throughput phenotyping platforms in plant genetic studies. Trends in Plant Science 12, 433-436.
60. Mounet F, Moing A, Kowalczyk M, et al. 2012. Down-regulation of a single auxin effux transport protein in tomato induces precocious fruit development. Journal of Experimental Botany 63, 4901-4917.
61. Muñoz-Fambuena N, Mesejo C, González-Mas MC, Primo-Millo E, Agustí M, Iglesias DJ. 2011. Fruit regulates seasonal expression of fowering genes in alternate-bearing 'Moncada' mandarin. Annals of Botany 108, 511-519.
62. Muñoz-Fambuena N, Mesejo C, González-Mas MC, Primo-Millo E, Agustí M, Iglesias DJ. 2012. Fruit load modulates fowering-related gene expression in buds of alternate-bearing 'Moncada' mandarin. Annals of Botany 110, 1109-1118.
63. Naor A, Naschitz S, Peres M, Gal Y. 2008. Responses of apple fruit size to tree water status and crop load. Tree Physiology 28, 1255-1261.
64. Nebauer SG, Renau-Morata B, Guardiola JL, Molina RV. 2011. Photosynthesis down-regulation precedes carbohydrate accumulation under sink limitation in Citrus. Tree Physiology 31, 169-177.
65. Obiadalla-Ali H, Fernie AR, Lytovchenko A, Kossmann J, Lloyd JR. 2004. Inhibition of chloroplastic fructose 1, 6-bisphosphatase in tomato fruits leads to decreased fruit size, but only small changes in carbohydrate metabolism. Planta 219, 533-540.
66. Pastore C, Zenoni S, Fasoli M, Pezzotti M, Tornielli GB, Filippetti I. 2013. Selective defoliation affects plant growth, fruit transcriptional ripening program and favonoid metabolism in grapevine. BMC Plant Biology 13, 30.
67. Pastore C, Zenoni S, Tornielli GB, Allegro G, Dal Santo S, Valentini G, Intrieri C, Pezzotti M, Filippetti I. 2011. Increasing the source/sink ratio in Vitis vinifera (cv Sangiovese) induces extensive transcriptome reprogramming and modifes berry ripening. BMC Genomics 12, 631.
68. Perrot-Rechenmann C. 2010. Cellular responses to auxin: division versus expansion. Cold Spring Harbor Perspectives in Biology 2, a001446.
69. Poiroux-Gonord F, Fanciullino AL, Poggi I, Urban L. 2013. Carbohydrate control over carotenoid build-up is conditional on fruit ontogeny in clementine fruits. Physiologia Plantarum 147, 417-431.
70. Prudent M, Bertin N, Génard M, Muños S, Rolland S, Garcia V, Petit J, Baldet P, Rothan C, Causse M. 2010. Genotype-dependent response to carbon availability in growing tomato fruit. Plant, Cell & Environment 33, 1186-1204.
71. Prudent M, Causse M, Génard M, Tripodi P, Grandillo S, Bertin N. 2009. Genetic and physiological analysis of tomato fruit weight and composition: infuence of carbon availability on QTL detection. Journal of Experimental Botany 60, 923-937.
72. Prudent M, Lecomte A, Bouchet JP, Bertin N, Causse M, Génard M. 2011. Combining ecophysiological modelling and quantitative trait locus analysis to identify key elementary processes underlying tomato fruit sugar concentration. Journal of Experimental Botany 62, 907-919.
73. Quilot B, Génard M, Kervella J, Lescourret F. 2002. Ecophysiological analysis of genotype variation in peach fruit growth. Journal of Experimental Botany 53, 1613-1625.
74. Quilot B, Génard M, Lescourret F, Kervella J. 2005a. Simulating genotypic variation of fruit quality in an advanced peach×Prunus davidiana cross. Journal of Experimental Botany 56, 3071-3081.
75. Quilot B, Kervella J, Génard M, Lescourret F. 2005b. Analysing the genetic control of peach fruit quality through an ecophysiological model combined with a QTL approach. Journal of Experimental Botany 56, 3083-3092.
76. Quilot-Turion B, Ould-Sidi MM, Kadrani A, Hilgert N, Génard M, Lescourret F. 2012. Optimization of parameters of the 'Virtual Fruit' model to design peach genotype for sustainable production systems. European Journal of Agronomy 42, 34-48.
77. Ragoussis J. 2009. Genotyping technologies for genetic research. Annual Review Genomics and Human Genetics 10, 117-133.
78. Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR. 2012. Molecular regulation of seed and fruit set. Trends in Plant Science 17, 656-665.
79. Samach A, Smith HM. 2013. Constraints to obtaining consistent annual yields in perennials. II: Environment and fruit load affect induction of fowering. Plant Science 207, 168-176.
80. Schauer N, Semel Y, Roessner U, et al. 2006. Comprehensive metabolic profling and phenotyping of interspecifc introgression lines for tomato improvement. Nature Biotechnology 24, 447-454.
81. Scorza R, May LG, Purnell B, Upchurch B. 1991. Differences in number and area of mesocarp cells between small-and large-fruited peach cultivars. Journal of the American Society of Horticultural Science 116, 861-864.
82. Shalom L, Samuels S, Zur N, Shlizerman L, Zemach H, Weissberg M, Ophir R, Blumwald E, Sadka A. 2012. Alternate bearing in citrus: changes in the expression of fowering control genes and in global gene expression in ON-versus OFF-crop trees. PLoS One October 7, e46930.
83. Smith HM, Samach A. 2013. Constraints to obtaining consistent annual yields in perennial tree crops. I: heavy fruit load dominates over vegetative growth. Plant Science 207, 158-167.
84. Struik PC, Cassman KG, Koornneef M. 2007. A dialogue on interdisciplinary collaboration to bridge the gap between plant genomics and crop sciences. In: Spiertz JHJ, Struik PC, van Laar HH, eds. Scale and complexity in plant systems research: gene-plant-crop relations. The Netherlands: Springer, 319-328.
85. Struik PC, Yin X, de Visser P. 2005. Complex quality traits: now time to model. Trends in Plant Science 10, 513-516.
86. Syvertsen JP, Goñi C, Otero A. 2003. Fruit load and canopy shading affect leaf characteristics and net gas exchange of 'Spring' navel orange trees. Tree Physiology 23, 899-906.
87. Tanksley SD. 2004. The genetic, developmental, and molecular bases of fruit size and shape variation in tomato. Plant Cell 16, S181-S189.
88. Tardieu F. 2003. Virtual plants: modelling as a tool for the genomics of tolerance to water defcit. Trends in Plant Science 8, 9-14.
89. Telef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P. 2006. Sucrose defciency delays lycopene accumulation in tomato fruit pericarp discs. Plant Molecular Biology 62, 453-469
90. Tuberosa R. 2012. Phenotyping for drought tolerance of crops in the genomics era. Frontiers in Physiology 3, 347.
91. Valantin M, Gary C, Vaissière BE, Tchamitchian M, Bruneli B. 1998. Changing sink demand affects the area but not the specifc activity of assimilate sources in cantaloupe (Cucumis melo L.). Annals of Botany 82, 711-719.
92. van Eeuwijk FA, Bink MCAM, Chenu K, Chapman SC. 2010. Detections and use of QTL for complex traits in multiple environments. Current Opinion in Plant Biology 13, 193-205.
93. Wang H, Jones B, Li Z, Frasse P, Delalande C, Regad F, Chaabouni S, Latché A, Pech JC, Bouzayen M. 2005. The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17, 2676-2692.
94. Wang H, Misztal I, Aguilar I, Legarra A, Muir WM. 2012. Genome-wide association mapping including phenotypes from relatives without genotypes. Genetics Research, Cambridge 94, 73-83.
95. Wang L, Ruan YL. 2013. Regulation of cell division and expansion by sugar and auxin signaling. Frontiers in Plant Science 4, 163.
96. Wünsche JN, Ferguson IB. 2005. Crop load interactions in apple. Horticultural Reviews 31, 231-290.
97. Wünsche JN, Greer DH, Laing WA, Palmer JW. 2005. Physiological and biochemical leaf and tree responses to crop load in apple. Tree Physiology 25, 1253-1263.
98. Yin X, Struik PC. 2008. Applying modelling experiences from the past to shape crop systems biology: the need to converge crop physiology and functional genomics. New Phytologist 179, 629-642.
99. Yin X, Struik PC. 2010. Modelling the crop: from system dynamics to systems biology. Journal of Experimental Botany 61, 2171-2183.
100. Yin X, Struik PC, Kropff MJ. 2004. Role of crop physiology in predicting gene-to-phenotype relationships. Trends in Plant Science 9, 426-432.
101. 13C-photosynthate accumulation in Japanese pear fruit during the period of rapid fruit growth is limited by the sink strength of fruit rather than by the transport capacity of the pedicel. Journal of Experimental Botany 56, 2713-2719.
102. Zhang C, Tanabe K, Wang S, Tamura F, Yoshida A, Matsumoto K. 2006. The impact of cell division and cell enlargement on the evolution of fruit size in Pyrus pyrifolia. Annals of Botany 98, 537-543.