Quantitative trait loci affecting reproductive phenology in peach

Background: The reproductive phenology of perennial plants in temperate climates is largely conditioned by the duration of bud dormancy, and fruit developmental processes. Bud dormancy release and bud break depends on the perception of cumulative chilling and heat during the bud development. The objective of this work was to identify new quantitative trait loci (QTLs) associated to temperature requirements for bud dormancy release and flowering and to fruit harvest date, in a segregating population of peach. Results: We have identified QTLs for nine traits related to bud dormancy, flowering and fruit harvest in an intraspecific hybrid population of peach in two locations differing in chilling time accumulation. QTLs were located in a genetic linkage map of peach based on single nucleotide polymorphism (SNP) markers for eight linkage groups (LGs) of the peach genome sequence. QTLs for chilling requirements for dormancy release and blooming clustered in seven different genomic regions that partially coincided with loci identified in previous works. The most significant QTL for chilling requirements mapped to LG1, close to the evergrowing locus. QTLs for heat requirement related traits were distributed in nine genomic regions, four of them co-localizing with QTLs for chilling requirement trait. Two major loci in LG4 and LG6 determined fruit harvest time. Conclusions: We identified QTLs associated to nine traits related to the reproductive phenology in peach. A search of candidate genes for these QTLs rendered different genes related to flowering regulation, chromatin modification and hormone signalling. A better understanding of the genetic factors affecting crop phenology might help scientists and breeders to predict changes in genotype performance in a context of global climate change.We thank Matilde Gonzalez for technical assistance. This work was supported by the Instituto Nacional de Investigacion y Tecnologia Agraria y Alimentaria (INIA)-FEDER (grant no. RTA2007-00060), and the Ministry of Science and Innovation of Spain (grant no. AGL2010-20595).Romeu, J.; Monforte Gilabert, AJ.; Sánchez, G.; Granell Richart, A.; Garcia-Brunton, J.; Badenes, M.; Rios Garcia, G. (2014). Quantitative trait loci affecting reproductive phenology in peach. BMC Plant Biology. 14(52):1-16. https://doi.org/10.1186/1471-2229-14-521161452Rohde, A., & Bhalerao, R. P. (2007). Plant dormancy in the perennial context. Trends in Plant Science, 12(5), 217-223. doi:10.1016/j.tplants.2007.03.012Coville, F. V. (1920). The Influence of Cold in Stimulating the Growth of Plants. Proceedings of the National Academy of Sciences, 6(7), 434-435. doi:10.1073/pnas.6.7.434Chuine, I. (2010). Why does phenology drive species distribution? Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1555), 3149-3160. doi:10.1098/rstb.2010.0142Hänninen, H., & Tanino, K. (2011). Tree seasonality in a warming climate. Trends in Plant Science, 16(8), 412-416. doi:10.1016/j.tplants.2011.05.001Yu, H., Luedeling, E., & Xu, J. (2010). Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proceedings of the National Academy of Sciences, 107(51), 22151-22156. doi:10.1073/pnas.1012490107Nicotra, A. B., Atkin, O. K., Bonser, S. P., Davidson, A. M., Finnegan, E. J., Mathesius, U., … van Kleunen, M. (2010). Plant phenotypic plasticity in a changing climate. Trends in Plant Science, 15(12), 684-692. doi:10.1016/j.tplants.2010.09.008Rohde, A., Storme, V., Jorge, V., Gaudet, M., Vitacolonna, N., Fabbrini, F., … Bastien, C. (2010). Bud set in poplar - genetic dissection of a complex trait in natural and hybrid populations. New Phytologist, 189(1), 106-121. doi:10.1111/j.1469-8137.2010.03469.xFabbrini, F., Gaudet, M., Bastien, C., Zaina, G., Harfouche, A., Beritognolo, I., … Sabatti, M. (2012). Phenotypic plasticity, QTL mapping and genomic characterization of bud set in black poplar. BMC Plant Biology, 12(1), 47. doi:10.1186/1471-2229-12-47Celton, J.-M., Martinez, S., Jammes, M.-J., Bechti, A., Salvi, S., Legave, J.-M., & Costes, E. (2011). Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. New Phytologist, 192(2), 378-392. doi:10.1111/j.1469-8137.2011.03823.xQuilot, B., Wu, B. H., Kervella, J., G�nard, M., Foulongne, M., & Moreau, K. (2004). QTL analysis of quality traits in an advanced backcross between Prunus persica cultivars and the wild relative species P. davidiana. Theoretical and Applied Genetics, 109(4), 884-897. doi:10.1007/s00122-004-1703-zDirlewanger, E., Quero-García, J., Le Dantec, L., Lambert, P., Ruiz, D., Dondini, L., … Arús, P. (2012). Comparison of the genetic determinism of two key phenological traits, flowering and maturity dates, in three Prunus species: peach, apricot and sweet cherry. Heredity, 109(5), 280-292. doi:10.1038/hdy.2012.38Olukolu, B. A., Trainin, T., Fan, S., Kole, C., Bielenberg, D. G., Reighard, G. L., … Holland, D. (2009). Genetic linkage mapping for molecular dissection of chilling requirement and budbreak in apricot (Prunus armeniacaL.). Genome, 52(10), 819-828. doi:10.1139/g09-050Fan, S., Bielenberg, D. G., Zhebentyayeva, T. N., Reighard, G. L., Okie, W. R., Holland, D., & Abbott, A. G. (2009). Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytologist, 185(4), 917-930. doi:10.1111/j.1469-8137.2009.03119.xJiménez, S., Li, Z., Reighard, G. L., & Bielenberg, D. G. (2010). Identification of genes associated with growth cessation and bud dormancy entrance using a dormancy-incapable tree mutant. BMC Plant Biology, 10(1), 25. doi:10.1186/1471-2229-10-25Verde, I., Bassil, N., Scalabrin, S., Gilmore, B., Lawley, C. T., Gasic, K., … Peace, C. (2012). Development and Evaluation of a 9K SNP Array for Peach by Internationally Coordinated SNP Detection and Validation in Breeding Germplasm. PLoS ONE, 7(4), e35668. doi:10.1371/journal.pone.0035668Leida, C., Terol, J., Marti, G., Agusti, M., Llacer, G., Badenes, M. L., & Rios, G. (2010). Identification of genes associated with bud dormancy release in Prunus persica by suppression subtractive hybridization. Tree Physiology, 30(5), 655-666. doi:10.1093/treephys/tpq008Leida, C., Conesa, A., Llácer, G., Badenes, M. L., & Ríos, G. (2011). Histone modifications and expression of DAM6 gene in peach are modulated during bud dormancy release in a cultivar-dependent manner. New Phytologist, 193(1), 67-80. doi:10.1111/j.1469-8137.2011.03863.xHolec, S., & Berger, F. (2011). Polycomb Group Complexes Mediate Developmental Transitions in Plants. Plant Physiology, 158(1), 35-43. doi:10.1104/pp.111.186445Pandey, R. (2002). Analysis of histone acetyltransferase and histone deacetylase families of Arabidopsis thaliana suggests functional diversification of chromatin modification among multicellular eukaryotes. Nucleic Acids Research, 30(23), 5036-5055. doi:10.1093/nar/gkf660Verde, I., Abbott, A. G., Scalabrin, S., Jung, S., Shu, S., … Grimwood, J. (2013). The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nature Genetics, 45(5), 487-494. doi:10.1038/ng.2586Jiménez, S., Lawton-Rauh, A. L., Reighard, G. L., Abbott, A. G., & Bielenberg, D. G. (2009). Phylogenetic analysis and molecular evolution of the dormancy associated MADS-box genes from peach. BMC Plant Biology, 9(1), 81. doi:10.1186/1471-2229-9-81Li, Z., Reighard, G. L., Abbott, A. G., & Bielenberg, D. G. (2009). Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. Journal of Experimental Botany, 60(12), 3521-3530. doi:10.1093/jxb/erp195Jiménez, S., Reighard, G. L., & Bielenberg, D. G. (2010). Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate. Plant Molecular Biology, 73(1-2), 157-167. doi:10.1007/s11103-010-9608-5Yamane, H., Ooka, T., Jotatsu, H., Hosaka, Y., Sasaki, R., & Tao, R. (2011). Expressional regulation of PpDAM5 and PpDAM6, peach (Prunus persica) dormancy-associated MADS-box genes, by low temperature and dormancy-breaking reagent treatment. Journal of Experimental Botany, 62(10), 3481-3488. doi:10.1093/jxb/err028Leida, C., Conejero, A., Arbona, V., Gómez-Cadenas, A., Llácer, G., Badenes, M. L., & Ríos, G. (2012). Chilling-Dependent Release of Seed and Bud Dormancy in Peach Associates to Common Changes in Gene Expression. PLoS ONE, 7(5), e35777. doi:10.1371/journal.pone.0035777Horvath, D. P., Sung, S., Kim, D., Chao, W., & Anderson, J. (2010). Characterization, expression and function of DORMANCY ASSOCIATED MADS-BOX genes from leafy spurge. Plant Molecular Biology, 73(1-2), 169-179. doi:10.1007/s11103-009-9596-5Sasaki, R., Yamane, H., Ooka, T., Jotatsu, H., Kitamura, Y., Akagi, T., & Tao, R. (2011). Functional and Expressional Analyses of PmDAM Genes Associated with Endodormancy in Japanese Apricot. Plant Physiology, 157(1), 485-497. doi:10.1104/pp.111.181982Hemming, M. N., & Trevaskis, B. (2011). Make hay when the sun shines: The role of MADS-box genes in temperature-dependant seasonal flowering responses. Plant Science, 180(3), 447-453. doi:10.1016/j.plantsci.2010.12.001He, Y. (2012). Chromatin regulation of flowering. Trends in Plant Science, 17(9), 556-562. doi:10.1016/j.tplants.2012.05.001Santamaría, M., Hasbún, R., Valera, M., Meijón, M., Valledor, L., Rodríguez, J. L., … Rodríguez, R. (2009). Acetylated H4 histone and genomic DNA methylation patterns during bud set and bud burst in Castanea sativa. Journal of Plant Physiology, 166(13), 1360-1369. doi:10.1016/j.jplph.2009.02.014Santamaría, M. E., Rodríguez, R., Cañal, M. J., & Toorop, P. E. (2011). Transcriptome analysis of chestnut (Castanea sativa) tree buds suggests a putative role for epigenetic control of bud dormancy. Annals of Botany, 108(3), 485-498. doi:10.1093/aob/mcr185Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., & Abrams, S. R. (2010). Abscisic Acid: Emergence of a Core Signaling Network. Annual Review of Plant Biology, 61(1), 651-679. doi:10.1146/annurev-arplant-042809-112122Santiago, J., Rodrigues, A., Saez, A., Rubio, S., Antoni, R., Dupeux, F., … Rodriguez, P. L. (2009). Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. The Plant Journal, 60(4), 575-588. doi:10.1111/j.1365-313x.2009.03981.xHorvath, D. P., Anderson, J. V., Chao, W. S., & Foley, M. E. (2003). Knowing when to grow: signals regulating bud dormancy. Trends in Plant Science, 8(11), 534-540. doi:10.1016/j.tplants.2003.09.013Ruttink, T., Arend, M., Morreel, K., Storme, V., Rombauts, S., Fromm, J., … Rohde, A. (2007). A Molecular Timetable for Apical Bud Formation and Dormancy Induction in Poplar. The Plant Cell, 19(8), 2370-2390. doi:10.1105/tpc.107.052811Melzer, S., Kampmann, G., Chandler, J., & Apel, K. (1999). FPF1 modulates the competence to flowering in Arabidopsis. The Plant Journal, 18(4), 395-405. doi:10.1046/j.1365-313x.1999.00461.xSchubert, D., Primavesi, L., Bishopp, A., Roberts, G., Doonan, J., Jenuwein, T., & Goodrich, J. (2006). Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27. The EMBO Journal, 25(19), 4638-4649. doi:10.1038/sj.emboj.7601311Zemach, A., Kim, M. Y., Hsieh, P.-H., Coleman-Derr, D., Eshed-Williams, L., Thao, K., … Zilberman, D. (2013). The Arabidopsis Nucleosome Remodeler DDM1 Allows DNA Methyltransferases to Access H1-Containing Heterochromatin. Cell, 153(1), 193-205. doi:10.1016/j.cell.2013.02.033Sridha, S., & Wu, K. (2006). Identification ofAtHD2Cas a novel regulator of abscisic acid responses in Arabidopsis. The Plant Journal, 46(1), 124-133. doi:10.1111/j.1365-313x.2006.02678.xKim, D.-H., & Sung, S. (2010). The Plant Homeo Domain finger protein, VIN3-LIKE 2, is necessary for photoperiod-mediated epigenetic regulation of the floral repressor, MAF5. Proceedings of the National Academy of Sciences, 107(39), 17029-17034. doi:10.1073/pnas.1010834107Jiang, D., Kong, N. C., Gu, X., Li, Z., & He, Y. (2011). Arabidopsis COMPASS-Like Complexes Mediate Histone H3 Lysine-4 Trimethylation to Control Floral Transition and Plant Development. PLoS Genetics, 7(3), e1001330. doi:10.1371/journal.pgen.1001330Lu, F., Cui, X., Zhang, S., Jenuwein, T., & Cao, X. (2011). Arabidopsis REF6 is a histone H3 lysine 27 demethylase. Nature Genetics, 43(7), 715-719. doi:10.1038/ng.854Yu, C.-W., Liu, X., Luo, M., Chen, C., Lin, X., Tian, G., … Wu, K. (2011). HISTONE DEACETYLASE6 Interacts with FLOWERING LOCUS D and Regulates Flowering in Arabidopsis. Plant Physiology, 156(1), 173-184. doi:10.1104/pp.111.174417Weigel, D., Alvarez, J., Smyth, D. R., Yanofsky, M. F., & Meyerowitz, E. M. (1992). LEAFY controls floral meristem identity in Arabidopsis. Cell, 69(5), 843-859. doi:10.1016/0092-8674(92)90295-nYang, Z., Tian, L., Latoszek-Green, M., Brown, D., & Wu, K. (2005). Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Molecular Biology, 58(4), 585-596. doi:10.1007/s11103-005-7294-5Bonghi, C., Trainotti, L., Botton, A., Tadiello, A., Rasori, A., Ziliotto, F., … Ramina, A. (2011). A microarray approach to identify genes involved in seed-pericarp cross-talk and development in peach. BMC Plant Biology, 11(1), 107. doi:10.1186/1471-2229-11-107Wang, A., Tan, D., Takahashi, A., Zhong Li, T., & Harada, T. (2007). MdERFs, two ethylene-response factors involved in apple fruit ripening. Journal of Experimental Botany, 58(13), 3743-3748. doi:10.1093/jxb/erm224Manning, K., Tör, M., Poole, M., Hong, Y., Thompson, A. J., King, G. J., … Seymour, G. B. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics, 38(8), 948-952. doi:10.1038/ng1841Pirona, R., Eduardo, I., Pacheco, I., Da Silva Linge, C., Miculan, M., Verde, I., … Rossini, L. (2013). Fine mapping and identification of a candidate gene for a major locus controlling maturity date in peach. BMC Plant Biology, 13(1), 166. doi:10.1186/1471-2229-13-166Maruyama-Nakashita, A., Nakamura, Y., Tohge, T., Saito, K., & Takahashi, H. (2006). Arabidopsis SLIM1 Is a Central Transcriptional Regulator of Plant Sulfur Response and Metabolism. The Plant Cell, 18(11), 3235-3251. doi:10.1105/tpc.106.046458Seymour, G., Poole, M., Manning, K., & King, G. J. (2008). Genetics and epigenetics of fruit development and ripening. Current Opinion in Plant Biology, 11(1), 58-63. doi:10.1016/j.pbi.2007.09.003Sánchez, G., Besada, C., Badenes, M. L., Monforte, A. J., & Granell, A. (2012). A Non-Targeted Approach Unravels the Volatile Network in Peach Fruit. PLoS ONE, 7(6), e38992. doi:10.1371/journal.pone.0038992Lander, E. S., Green, P., Abrahamson, J., Barlow, A., Daly, M. J., Lincoln, S. E., & Newburg, L. (1987). MAPMAKER: An interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics, 1(2), 174-181. doi:10.1016/0888-7543(87)90010-3Voorrips, R. E. (2002). MapChart: Software for the Graphical Presentation of Linkage Maps and QTLs. Journal of Heredity, 93(1), 77-78. doi:10.1093/jhered/93.1.7