Mapping and identification of genetic loci affecting earliness of bolting and flowering in lettuce.
Journal
TAG. Theoretical and applied genetics. Theoretische und angewandte Genetik
ISSN: 1432-2242
Titre abrégé: Theor Appl Genet
Pays: Germany
ID NLM: 0145600
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
received:
16
04
2021
accepted:
25
06
2021
pubmed:
2
7
2021
medline:
2
10
2021
entrez:
1
7
2021
Statut:
ppublish
Résumé
Photoperiod and temperature conditions elicit different genetic regulation over lettuce bolting and flowering. This study identifies environment-specific QTLs and putative genes and provides information for genetic marker assay. Bolting, defined as stem elongation, marks the plant life cycle transition from vegetative to reproductive stage. Lettuce is grown for its leaf rosettes, and premature bolting may reduce crop quality resulting in economic losses. The transition to reproductive stage is a complex process that involves many genetic and environmental factors. In this study, the effects of photoperiod and ambient temperature on bolting and flowering regulation were studied by utilizing a lettuce mapping population to identify quantitative trait loci (QTL) and by gene expression analyses of genotypes with contrasting phenotypes. A recombinant inbred line (RIL) population, derived from a cross between PI 251246 (early bolting) and cv. Salinas (late bolting), was grown in four combinations of short (8 h) and long (16 h) days and low (20 °C) and high (35 °C) temperature. QTL models revealed both genetic (G) and environmental (E) effects, and GxE interactions. A major QTL for bolting and flowering time was found on chromosome 7 (qFLT7.2), and two candidate genes were identified by fine mapping, homology, and gene expression studies. In short days and high temperature conditions, qFLT7.2 had no effect on plant development, while several small-effect loci on chromosomes 2, 3, 6, 8, and 9 were associated with bolting and flowering. Of these, the QTL on chromosome 2, qBFr2.1, co-located with the Flowering Locus T (LsFT) gene. Polymorphisms between parent genotypes in the promotor region may explain identified gene expression differences and were used to design a genetic marker which may be used to identify the late bolting trait.
Identifiants
pubmed: 34196730
doi: 10.1007/s00122-021-03898-9
pii: 10.1007/s00122-021-03898-9
doi:
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3319-3337Subventions
Organisme : Agricultural Research Institute, California State University
ID : 14-01-008
Organisme : CSRD VA
ID : 1
Pays : United States
Informations de copyright
© 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
Références
Adrian J, Farrona S, Reimer JJ et al (2010) cis-Regulatory elements and chromatin state coordinately control temporal and spatial expression of flowering locus t in arabidopsis. Plant Cell Online 22:1425–1440. https://doi.org/10.1105/tpc.110.074682
doi: 10.1105/tpc.110.074682
Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013. https://doi.org/10.1111/j.1365-313X.2010.04148.x
doi: 10.1111/j.1365-313X.2010.04148.x
pubmed: 20409274
Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639. https://doi.org/10.1038/nrg3291
doi: 10.1038/nrg3291
pubmed: 22898651
Ballerini ES, Kramer EM (2011) In the light of evolution: a reevaluation of conservation in the CO-FT regulon and its role in photoperiodic regulation of flowering time. Front Plant Sci 2:1–13. https://doi.org/10.3389/fpls.2011.00081
doi: 10.3389/fpls.2011.00081
Bao S, Hua C, Shen L, Yu H (2020) New insights into gibberellin signaling in regulating flowering in Arabidopsis. J Integr Plant Biol 62:118–131. https://doi.org/10.1111/jipb.12892
doi: 10.1111/jipb.12892
pubmed: 31785071
Blackman BK, Strasburg JL, Raduski AR et al (2010) The role of recently derived ft paralogs in sunflower domestication. Curr Biol 20:629–635. https://doi.org/10.1016/j.cub.2010.01.059
doi: 10.1016/j.cub.2010.01.059
pubmed: 20303265
pmcid: 2898918
Blázquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171. https://doi.org/10.1038/ng1085
doi: 10.1038/ng1085
pubmed: 12548286
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops-what did we learn from Arabidopsis? Curr Opin Biotechnol 32:121–129. https://doi.org/10.1016/j.copbio.2014.11.023
doi: 10.1016/j.copbio.2014.11.023
pubmed: 25553537
Borowski JM, Galli V, da Silva MR et al (2014) Selection of candidate reference genes for real-time PCR studies in lettuce under abiotic stresses. Planta 239:1187–1200. https://doi.org/10.1007/s00425-014-2041-2
doi: 10.1007/s00425-014-2041-2
pubmed: 24573225
Bouché F, Lobet G, Tocquin P, Périlleux C (2016) FLOR-ID: an interactive database of flowering-time gene networks in Arabidopsis thaliana. Nucleic Acids Res 44:D1167–D1171. https://doi.org/10.1093/nar/gkv1054
doi: 10.1093/nar/gkv1054
pubmed: 26476447
Broman KW, Speed TP (2002) A model selection approach for the identification of quantitative trait loci in experimental crosses. J R Stat Soc B 64:641–656. https://doi.org/10.1534/genetics.109.112912
doi: 10.1534/genetics.109.112912
Broman KW, Wu H, Sen Ś, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890. https://doi.org/10.1093/bioinformatics/btg112
doi: 10.1093/bioinformatics/btg112
pubmed: 12724300
Capovilla G, Schmid M, Posé D (2015) Control of flowering by ambient temperature. J Exp Bot 66:59–69. https://doi.org/10.1093/jxb/eru416
doi: 10.1093/jxb/eru416
pubmed: 25326628
Catt SC, Braich S, Kaur S, Paull JG (2017) QTL detection for flowering time in faba bean and the responses to ambient temperature and photoperiod. Euphytica 213:1–13. https://doi.org/10.1007/s10681-017-1910-8
doi: 10.1007/s10681-017-1910-8
Chen Z, Han Y, Ning K et al (2018a) Inflorescence development and the role of lsft in regulating bolting in lettuce (Lactuca sativa L.). Front Plant Sci 8:1–10. https://doi.org/10.3389/fpls.2017.02248
doi: 10.3389/fpls.2017.02248
Chen Z, Zhao W, Ge D et al (2018b) LCM-seq reveals the crucial role of LsSOC1 in heat-promoted bolting of lettuce (Lactuca sativa L.). Plant J 95:516–528. https://doi.org/10.1111/tpj.13968
doi: 10.1111/tpj.13968
pubmed: 29772090
Cheng XF, Wang ZY (2005) Overexpression of COL9, a CONSTANS-LIKE gene, delays flowering by reducing expression of CO and FT in Arabidopsis thaliana. Plant J 43:758–768. https://doi.org/10.1111/j.1365-313X.2005.02491.x
doi: 10.1111/j.1365-313X.2005.02491.x
pubmed: 16115071
Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719. https://doi.org/10.1111/tpj.13461
doi: 10.1111/tpj.13461
pubmed: 27995671
Corbesier L, Vincent C, Jang S et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science. https://doi.org/10.1126/science.1141752
doi: 10.1126/science.1141752
pubmed: 17446353
Czechowski T, Stitt M, Altmann T et al (2005) Genome-wide identification and testing of superior reference genes for transcript normalization. Plant Physiol 139:5–17. https://doi.org/10.1104/pp.105.063743.1
doi: 10.1104/pp.105.063743.1
pubmed: 16166256
pmcid: 1203353
Davuluri RV, Sun H, Palaniswamy SK et al (2003) AGRIS: arabidopsis Gene Regulatory Information Server, an information resource of Arabidopsis cis-regulatory elements and transcription factors. BMC Bioinform 4:1–11. https://doi.org/10.1186/1471-2105-4-25
doi: 10.1186/1471-2105-4-25
Elshire RJ, Glaubitz JC, Sun Q et al (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6:1–10. https://doi.org/10.1371/journal.pone.0019379
doi: 10.1371/journal.pone.0019379
Feenstra B, Skovgaard IM, Broman KW (2006) Mapping quantitative trait loci by an extension of the Haley-Knott regression method using estimating equations. Genetics 173:2269–2282. https://doi.org/10.1534/genetics.106.058537
doi: 10.1534/genetics.106.058537
pubmed: 16702423
pmcid: 1569686
Fernández V, Takahashi Y, Le Gourrierec J, Coupland G (2016) Photoperiodic and thermosensory pathways interact through CONSTANS to promote flowering at high temperature under short days. Plant J 86:426–440. https://doi.org/10.1111/tpj.13183
doi: 10.1111/tpj.13183
pubmed: 27117775
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in arabidopsis. Cell 141:3–5. https://doi.org/10.1016/j.cell.2010.04.024
doi: 10.1016/j.cell.2010.04.024
Franklin KA, Davis SJ, Stoddart WM et al (2003) Mutant analyses define multiple roles for phytochrome c in arabidopsis photomorphogenesis. Plant Cell Online 15:1981–1989. https://doi.org/10.1105/tpc.015164
doi: 10.1105/tpc.015164
Fukuda M, Matsuo S, Kikuchi K et al (2009) The endogenous level of GA1is upregulated by high temperature during stem elongation in lettuce through LsGA3ox1 expression. J Plant Physiol 166:2077–2084. https://doi.org/10.1016/j.jplph.2009.06.003
doi: 10.1016/j.jplph.2009.06.003
pubmed: 19576660
Fukuda M, Matsuo S, Kikuchi K et al (2011) Isolation and functional characterization of the FLOWERING LOCUS T homolog, the LsFT gene, in lettuce. J Plant Physiol 168:1602–1607. https://doi.org/10.1016/j.jplph.2011.02.004
doi: 10.1016/j.jplph.2011.02.004
pubmed: 21392841
Fukuda M, Yanai Y, Nakano Y et al (2017) Isolation and gene expression analysis of flowering-related genes in lettuce (Lactuca sativa L.). Hortic J 86:340–348. https://doi.org/10.2503/hortj.OKD-036
doi: 10.2503/hortj.OKD-036
Glaubitz JC, Casstevens TM, Lu F et al (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE. https://doi.org/10.1371/journal.pone.0090346
doi: 10.1371/journal.pone.0090346
pubmed: 24587335
pmcid: 3938676
Grube R, Ryder E (2004) Identification of Lettuce (Lactuca sativa L.) Germplasm with Genetic Resistance to Drop Caused by Sclerotinia minor. J Am Soc Hortic Sci 129:70–76
doi: 10.21273/JASHS.129.1.0070
GuoYou Y, Ogbonnaya F, van Ginkel M (2010) Marker-assisted recurrent backcrossing in cultivar development. Molecular plant breeding: principle, method and application. Studium Press LLC, Houston, pp 295–319
Han Y, Chen Z, Lv S et al (2016) MADS-box genes and gibberellins regulate bolting in lettuce (Lactuca sativa L.). Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.01889
doi: 10.3389/fpls.2016.01889
Han R, Truco MJ, Lavelle DO, Michelmore RW (2021) A composite analysis of flowering time regulation in lettuce. Front Plant Sci 12:1–14. https://doi.org/10.3389/fpls.2021.632708
doi: 10.3389/fpls.2021.632708
Hartman Y, Hooftman DAP, Uwimana B et al (2012) Genomic regions in crop-wild hybrids of lettuce are affected differently in different environments: implications for crop breeding. Evol Appl 5:629–640. https://doi.org/10.1111/j.1752-4571.2012.00240.x
doi: 10.1111/j.1752-4571.2012.00240.x
pubmed: 23028403
pmcid: 3461145
Hartman Y, Hooftman DAP, Eric Schranz M, van Tienderen PH (2013) QTL analysis reveals the genetic architecture of domestication traits in Crisphead lettuce. Genet Resour Crop Evol 60:1487–1500. https://doi.org/10.1007/s10722-012-9937-0
doi: 10.1007/s10722-012-9937-0
Hayashi E, Aoyama N, Wu Y et al (2007) Multiplexed, quantitative gene expression analysis for lettuce seed germination on GenomeLab™ GeXP Genetic Analysis System. Beckman-Coulter Application Information-10295A. https://sciex.jp/content/dam/SCIEX/pdf/tech-notes/all/A-10295A-c.pdf
Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27:297–300. https://doi.org/10.1093/nar/27.1.297
doi: 10.1093/nar/27.1.297
pubmed: 9847208
pmcid: 148163
Huo H, Wei S, Bradford KJ (2016) DELAY OF GERMINATION1 ( DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci 113:E2199–E2206. https://doi.org/10.1073/pnas.1600558113
doi: 10.1073/pnas.1600558113
pubmed: 27035986
pmcid: 4839450
Ito H, Kato T, Konno Y (1963) Factors associated with the Flower Induction in Lettuce. Tohoku J Agric Res 14:51–65
doi: 10.1071/AR9630051
Jenni S, Truco MJ, Michelmore RW (2013) Quantitative trait loci associated with tipburn, heat stress-induced physiological disorders, and maturity traits in crisphead lettuce. Theor Appl Genet 126:3065–3079. https://doi.org/10.1007/s00122-013-2193-7
doi: 10.1007/s00122-013-2193-7
Jeuken MJW, Lindhout P (2004) The development of lettuce backcross inbred lines (BILs) for exploitation of the Lactuca saligna (wild lettuce) germplasm. Theor Appl Genet 109:394–401. https://doi.org/10.1007/s00122-004-1643-7
doi: 10.1007/s00122-004-1643-7
pubmed: 15103409
Kendrick RE, Kronenberg GHM (1994) Photomorphogenesis in plants. Springer, Netherlands. https://doi.org/10.1007/978-94-011-1884-2
doi: 10.1007/978-94-011-1884-2
Kim JJ, Lee JH, Kim W et al (2012) The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis. Plant Physiol 159:461–478. https://doi.org/10.1104/pp.111.192369
doi: 10.1104/pp.111.192369
pubmed: 22427344
pmcid: 3375978
Kim W, Park TI, Yoo SJ et al (2013) Generation and analysis of a complete mutant set for the Arabidopsis FT/TFL1 family shows specific effects on thermo-sensitive flowering regulation. J Exp Bot 64:1715–1729. https://doi.org/10.1093/jxb/ert036
doi: 10.1093/jxb/ert036
pubmed: 23404901
pmcid: 3617836
Komeda Y (2004) Genetic regulation of time to flower in arabidopsis thaliana. Annu Rev Plant Biol 55:521–535. https://doi.org/10.1146/annurev.arplant.55.031903.141644
doi: 10.1146/annurev.arplant.55.031903.141644
pubmed: 15377230
Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49:345–370. https://doi.org/10.1002/9781119409144.ch22
doi: 10.1002/9781119409144.ch22
Kumar SV, Lucyshyn D, Jaeger KE et al (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245. https://doi.org/10.1038/nature10928
doi: 10.1038/nature10928
pubmed: 22437497
pmcid: 4972390
Kumimoto RW, Adam L, Hymus GJ et al (2008) The nuclear factor Y subunits NF-YB2 and NF-YB3 play additive roles in the promotion of flowering by inductive long-day photoperiods in Arabidopsis. Planta 228:709–723. https://doi.org/10.1007/s00425-008-0773-6
doi: 10.1007/s00425-008-0773-6
pubmed: 18600346
Kwon S, Simko I, Hellier B et al (2013) Genome-wide association of 10 horticultural traits with expressed sequence tag-derived SNP markers in a collection of lettuce lines. Crop J 1:25–33. https://doi.org/10.1016/j.cj.2013.07.014
doi: 10.1016/j.cj.2013.07.014
Lafta A, Turini T, Sandoya GV, Mou B (2017) Field Evaluation of green and red leaf lettuce genotypes in the imperial, san joaquin, and salinas valleys of california for heat tolerance and extension of the growing seasons. HortScience 52:40–48
doi: 10.21273/HORTSCI10835-16
Lee ON, Fukushima K, Park HY, Kawabata S (2021) QTL analysis of stem elongation and flowering time in lettuce using genotyping-by-sequencing. Genes 12(6):947. https://doi.org/10.3390/genes12060947
doi: 10.3390/genes12060947
pubmed: 34205694
pmcid: 8234873
Letunic I, Bork P (2018) 20 years of the SMART protein domain annotation resource. Nucleic Acids Res 46:D493–D496. https://doi.org/10.1093/nar/gkx922
doi: 10.1093/nar/gkx922
pubmed: 29040681
Liu L, Adrian J, Pankin A et al (2014) Induced and natural variation of promoter length modulates the photoperiodic response of FLOWERING LOCUS T. Nat Commun 5:1–9. https://doi.org/10.1038/ncomms5558
doi: 10.1038/ncomms5558
Liu X, Lv S, Liu R et al (2018) Transcriptomic analysis reveals the roles of gibberellin-regulated genes and transcription factors in regulating bolting in lettuce (Lactuca sativa L.). PLoS ONE 13:1–17. https://doi.org/10.1371/journal.pone.0191518
doi: 10.1371/journal.pone.0191518
Maldonado C, Mora F, Bengosi Bertagna FA et al (2019) SNP- and haplotype-based GWAS of flowering-related traits in maize with network-assisted gene prioritization. Agronomy. https://doi.org/10.3390/agronomy9110725
doi: 10.3390/agronomy9110725
Mamo BE, Hayes RJ, Truco MJ et al (2019) The genetics of resistance to lettuce drop (Sclerotinia spp.) in lettuce in a recombinant inbred line population from Reine des Glaces × Eruption. Theor Appl Genet 132:2439–2460. https://doi.org/10.1007/s00122-019-03365-6
doi: 10.1007/s00122-019-03365-6
pubmed: 31165222
Mátyás KK, Hegedűs G, Taller J et al (2019) Different expression pattern of flowering pathway genes contribute to male or female organ development during floral transition in the monoecious weed Ambrosia artemisiifolia L. (Asteraceae). PeerJ. https://doi.org/10.7717/peerj.7421
doi: 10.7717/peerj.7421
pubmed: 31598422
pmcid: 6779118
McGinnis S, Madden TL (2004) BLAST: at the core of a powerful and diverse set of sequence analysis tools. Nucleic Acids Res 32:20–25. https://doi.org/10.1093/nar/gkh435
doi: 10.1093/nar/gkh435
Michaels SD, Amasino RM (2000) Memories of winter: Vernalization and the competence to flower. Plant Cell Environ 23:1145–1153. https://doi.org/10.1046/j.1365-3040.2000.00643.x
doi: 10.1046/j.1365-3040.2000.00643.x
Monte E, Alonso JM, Ecker JR et al (2003) Isolation and characterization of phyc mutants in arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15:1962–1980. https://doi.org/10.1105/tpc.012971.direction
doi: 10.1105/tpc.012971.direction
pubmed: 12953104
pmcid: 181324
Nakano Y, Higuchi Y, Sumitomo K, Hisamatsu T (2013) Flowering retardation by high temperature in chrysanthemums: Involvement of FLOWERING LOCUS T-like 3 gene repression. J Exp Bot 64:909–920. https://doi.org/10.1093/jxb/ers370
doi: 10.1093/jxb/ers370
pubmed: 23314814
pmcid: 3580808
Ning K, Han Y, Chen Z et al (2019) Genome - wide analysis of MADS - box family genes during flower development in lettuce. Plant Cell Environ 42:1868–1881. https://doi.org/10.1111/pce.13523
doi: 10.1111/pce.13523
pubmed: 30680748
Nishida H, Ishihara D, Ishii M et al (2013) Phytochrome C is a key factor controlling long-day flowering in barley. Plant Physiol 163:804–814. https://doi.org/10.1104/pp.113.222570
doi: 10.1104/pp.113.222570
pubmed: 24014575
pmcid: 3793059
Pearce S, Kippes N, Chen A et al (2016) RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways. BMC Plant Biol 16:1–19. https://doi.org/10.1186/s12870-016-0831-3
doi: 10.1186/s12870-016-0831-3
Pham VN, Kathare PK, Huq E (2018) Phytochromes and phytochrome interacting factors. Plant Physiol 176:1025–1038. https://doi.org/10.1104/pp.17.01384
doi: 10.1104/pp.17.01384
pubmed: 29138351
Putterill J, Varkonyi-Gasic E (2016) FT and florigen long-distance flowering control in plants. Curr Opin Plant Biol 33:77–82. https://doi.org/10.1016/j.pbi.2016.06.008
doi: 10.1016/j.pbi.2016.06.008
pubmed: 27348248
Putterill J, Laurie R, Macknight R (2004) It’s time to flower: the genetic control of flowering time. BioEssays 26:363–373. https://doi.org/10.1002/bies.20021
doi: 10.1002/bies.20021
pubmed: 15057934
Rappaport L, Wittwer S, Tukey H (1956) Seed vernalization and flowering in lettuce (Lactuca sativa). Nature. https://doi.org/10.1038/178051a0
doi: 10.1038/178051a0
Reyes-Chin-Wo S, Wang Z, Yang X et al (2017) Genome assembly with in vitro proximity ligation data and whole-genome triplication in lettuce. Nat Commun 8:1–11. https://doi.org/10.1038/ncomms14953
doi: 10.1038/ncomms14953
Romera-Branchat M, Andrés F, Coupland G (2014) Flowering responses to seasonal cues: what’s new? Curr Opin Plant Biol 21:120–127. https://doi.org/10.1016/j.pbi.2014.07.006
doi: 10.1016/j.pbi.2014.07.006
pubmed: 25072635
Ryder EJ (1983) Inheritance, linkage, and gene interaction studies in lettuce. J Am Soc Hortic Sci 108:985–991
Ryder EJ (1988) Early flowering in lettuce as influenced by a second flowering time gene and seasonal variation. J Am Soc Hortic Sci 113:456–460
Ryder EJ (1996) Ten lettuce genetic stocks with early flowering genes Ef-lef- 1 and Ef- 2ef-2. HortScience 31:473–475
doi: 10.21273/HORTSCI.31.3.473
Ryder EJ, Milligan DC (2005) Additional genes controlling flowering time in Lactuca sativa and L. serriola. J Amer Soc Hort Sci 130:448–453
doi: 10.21273/JASHS.130.3.448
Samach A, Coupland G (2000) Time measurement and the control of flowering in plants. BioEssays 22:38–47
doi: 10.1002/(SICI)1521-1878(200001)22:1<38::AID-BIES8>3.0.CO;2-L
Schwartz C, Balasubramanian S, Warthmann N et al (2009) Cis-regulatory changes at Flowering Locus T mediate natural variation in flowering responses of Arabidopsis thaliana. Genetics 183:723–732. https://doi.org/10.1534/genetics.109.104984
doi: 10.1534/genetics.109.104984
pubmed: 19652183
pmcid: 2766330
Sgamma T, Pape J, Massiah A, Jackson S (2016) Selection of reference genes for diurnal and developmental time-course real-time PCR expression analyses in lettuce. Plant Methods 12:1–9. https://doi.org/10.1186/S13007-016-0121-Y
doi: 10.1186/S13007-016-0121-Y
Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev 3:1745–1757. https://doi.org/10.1101/gad.3.11.1745
doi: 10.1101/gad.3.11.1745
pubmed: 2606345
Shin AY, Han YJ, Baek A et al (2016) Evidence that phytochrome functions as a protein kinase in plant light signalling. Nat Commun. https://doi.org/10.1038/ncomms11545
doi: 10.1038/ncomms11545
pubmed: 27991499
pmcid: 5187435
Silva EC, Maluf WR, Leal NR, Gomes LAA (1999) Inheritance of bolting tendency in lettuce Lactuca sativa L. Euphytica 109:1–7. https://doi.org/10.1023/A:1003698117689
doi: 10.1023/A:1003698117689
Simko I (2013) Marker-Assisted Selection for Disease Resistance in Lettuce. In: Rajeev KV, Tuberosa R (eds) Translational Genomics for Crop Breeding, Volume I: Biotic Stress. John Wiley & Sons Inc, First Edit, pp 267–289
doi: 10.1002/9781118728475.ch14
Simko I (2016) High-resolution DNA melting analysis in plant research. Trends Plant Sci 21:528–537. https://doi.org/10.1016/j.tplants.2016.01.004
doi: 10.1016/j.tplants.2016.01.004
pubmed: 26827247
Simonne A, Simonne E, Eitenmiller R, Coker CH (2002) Bitterness and composition of lettuce varieties grown in the southeastern United States. HortTechnology 12:721–726
doi: 10.21273/HORTTECH.12.4.721
Song YH, Ito S, Imaizumi T (2013) Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci 18:575–583. https://doi.org/10.1016/j.tplants.2013.05.003
doi: 10.1016/j.tplants.2013.05.003
pubmed: 23790253
pmcid: 3796012
Song YH, Shim JS, Kinmonth-Schultz HA, Imaizumi T (2015) Photoperiodic flowering: time measurement mechanisms in leaves. Annu Rev Plant Biol 66:441–464. https://doi.org/10.1146/annurev-arplant-043014-115555
doi: 10.1146/annurev-arplant-043014-115555
pubmed: 25534513
Sthapit Kandel J, Peng H, Hayes RJ et al (2020) Genome-wide association mapping reveals loci for shelf life and developmental rate of lettuce. Theor Appl Genet 133:1947–1966. https://doi.org/10.1007/s00122-020-03568-2
doi: 10.1007/s00122-020-03568-2
pubmed: 32123958
Terzaghi WB, Cashmore AR (1995) Light-regulated transcription. Annu Rev Plant Physiol Plant Mol Biol 46:445–474
doi: 10.1146/annurev.pp.46.060195.002305
Thompson RC (1943) Further studies on interspecific genetic relationships in Lactuca. J Agric Res 66:41–48
Umetsu A, Sawada Y, Mitsuhashi W et al (2011) Characterization of a loss-of-function mutant of gibberellin biosynthetic gene lsga3ox1 in lettuce. Biosci Biotechnol Biochem 75:2398–2400. https://doi.org/10.1271/bbb.110475
doi: 10.1271/bbb.110475
pubmed: 22146725
Vandesompele J, De Preter K, Pattyn F et al (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:34–41. https://doi.org/10.1186/gb-2002-3-7-research0034
doi: 10.1186/gb-2002-3-7-research0034
Vierstra RD, Davis SJ (2000) Bacteriophytochromes: new tools for understanding phytochrome signal transduction. Semin Cell Dev Biol 11:511–521. https://doi.org/10.1006/scdb.2000.0206
doi: 10.1006/scdb.2000.0206
pubmed: 11145881
Wang L, Xue J, Dai W et al (2019) Genome-wide identification, phylogenetic analysis, and expression profiling of constans-like (col) genes in vitis vinifera. J Plant Growth Regul 38:631–643. https://doi.org/10.1007/s00344-018-9878-8
doi: 10.1007/s00344-018-9878-8
Waycott W (1995) Photoperiodic response of genetically diverse lettuce accessions. J Am Soc Hortic Sci 120:460–467
doi: 10.21273/JASHS.120.3.460
Wien HC (2020) Lettuce. In: Wien HC, Stutzel H (eds) The physiology of vegetable crops, 2nd edn. CAB International, Wallingford, UK, pp 333–356
doi: 10.1079/9781786393777.0333
Wu W, Zhang Y, Zhang M et al (2018) The rice CONSTANS-like protein OsCOL15 suppresses flowering by promoting Ghd7 and repressing RID1. Biochem Biophys Res Commun 495:1349–1355. https://doi.org/10.1016/j.bbrc.2017.11.095
doi: 10.1016/j.bbrc.2017.11.095
pubmed: 29154991
Yoong F-Y, O’Brien LK, Truco MJ et al (2016) Genetic variation for thermotolerance in lettuce seed germination Is associated with temperature-sensitive regulation of ETHYLENE RESPONSE FACTOR1 ( ERF1). Plant Physiol 170:472–488. https://doi.org/10.1104/pp.15.01251
doi: 10.1104/pp.15.01251
pubmed: 26574598