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Regulation factors of lettuce bolting and flowering

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Post time 2021-12-7 11:57:27 | Show all posts |Read mode
(Contributed by Li Bo)

       Bolting and flowering isthe key transition from the vegetative to reproductive phase in higher plants,and is regulated by many genetic pathways responding to endogenous cues andenvironmental factors, including photoperiod, vernalization, gibberellin (GA),autonomous and age pathways[1,2]. In the Arabidopsis many genes havebeen implicated in flowering-time control according to isolation ofloss-of-function mutants or analysis of transgenic plants[2,3]. Boltingis a complex process that is subject to auto-feedback and is affected byseveral factors, like hormones[4], environment[5],carbohydrates[6], C/N ratio[7], light, temperature[8,9]and so on.
Premature bolting andflowering is an undesirable agricultural trait that causes great economic lossin vegetables such as lettuce, cabbage and radish[10,11,12]. Unlikemost other flowering plants, transition from vegetative to reproductive phasein lettuce is induced by high temperatures, and followed by rapid stemelongation (bolting) and flowering[13]. However, there are fewerstudies of molecular mechanism underlying the bolting and flowering in lettuce.
       Hanet al.[14] used a bolting resistant line S24 and a boltingsensitive line S39 for morphological, physiological, transcriptomic andproteomic comparisons. A total of 12204 genes were differentially expressed inS39 vs. S24. Line S39 was featured with largerleaves, higher levels of chlorophyll, soluble sugar, anthocyanin and auxin,consistent with its up-regulation of genes implicated in photosynthesis,oxidation-reduction and auxin actions. Proteomic analysis identified 30differentially accumulated proteins in lines S39 and S24 upon heat treatment,and 19 out of the 30 genes showed differential expression in the RNA-Seq data.Exogenous GA treatment promoted bolting in both S39 and S24, while 12 floweringpromoting MADS-box genes were specifically induced in line S39,suggesting that although GA regulates bolting in lettuce, it may be the MADS-boxgenes, not GA, that plays a major role in differing the bolting resistancebetween these two lettuce lines.
       Liu et al.[15] found transcription factors (TFs)regulated bolting in lettuce and the high GA contents in the leaves and IAA inthe stem promote bolting. TFs possibly modulate the expression of relatedgenes, such as those encoding hormones, potentially regulating bolting inlettuce. Significant changes in the high  temperature treated group wereobserved for C2H2 zinc finger, AP2-EREBP, and WRKY families, indicating thatthese TFs may play important roles in regulating bolting.
       Chen et al.[16] used laser capture microdissection, RNA sequencing,comparative transcriptomic analysi, molecular biology, developmental biology,and biochemical tools investigate the biological function of LsSOC1 inlettuce. LsSOC1 knockdown by RNA interference resulted in a significantdelay in the timing of bolting and insensitivity to high temperature, which indicatedthat LsSOC1 functions as an activator during heat-promoted bolting inlettuce. This study also found that two heat shock transcription factors, HsfA1eand HsfA4c, bound to the promoter of LsSOC1 to confirm that LsSOC1played an important role in heat-promoted bolting.
Liu et al.[17]found that high temperatures could facilitate the accumulation of GA in lettuceto induce bolting, with higher expression levels of two heat shock proteingenes LsHsp70-3701 and LsHsp70- 2711. Lower expression levels ofthese two genes could enhance bolting stem length of lettuce under hightemperatures. It was found that a calmodulin protein could interact withLsHsp70 proteins in a high-temperature stress cDNA library, which was constructedfor lettuce. Also, the Hsp70-calmodulin combination can be obtained at hightemperatures. According to these results, it can be speculated that theinteraction between Hsp70 and calmodulin could be induced under hightemperatures and higher GA contents can be obtained at the same time, whichmeans these two proteins may play a signifcant role in heat-induced boltingtolerance.
       Chen et al.[18] functionallyanalyzed the FLOWERING LOCUS T (LsFT) gene during boltingregulation in lettuce. The expression of LsFT was negatively correlatedwith bolting in different lettuce varieties, and was promoted by heattreatment. Overexpression of LsFT could recover the late-floweringphenotype of ft-2 mutant. Knockdown of LsFT by RNA interferencedramatically delayed bolting in lettuce, and failed to respond to hightemperature.
       Ning et al.[19] analyzedMADS‐box family genes by Genome‐wide analysis, found LsMADS55 isresponsive to heat and is specifically expressed in the inflorescence meristemand pappus bristles. The overexpression of LsMADS55 results in earlyflowering in Arabidopsis thaliana. Furthermore, observed that the heat shock factor LsHSFB2A‐1 can bind to the LsMADS55promoter in lettuce. Therefore, a model was proposed for the LsMADS‐regulatedfloral organ specification and heat‐induced flowering in lettuce.
       Han et al.[20]integrated results from past genetic and molecular studies for floweringtime in lettuce with orthology and functional inference from Arabidopsis. Atotal of 167 QTLs have been reported for bolting and flowering time in lettucein the past years. Merging QTLs with extensively overlapping intervals reducesthis number to 67. Bolting (green) and flowering (yellow) time QTLs are locatedon all nine lettuce chromosomes (Fig1 A). Physical location of 167 QTLsreported in a total of 56 field and greenhouse experiments (Fig1 B). Locationof lettuce orthologs of genes with flowering time function in Arabidopsis asshown in Fig1 C. Gene density of the lettuce genome as shown in Fig1 D.Flowering time orthologs within the same orthogroup are connected (Fig1 E).
                              
Fig 1  A Composite Analysis of Bolting and FloweringTime Regulation in Lettuce
Reference:
[1]Mouradov, A., Cremer, F., and Coupland, G. Control of flowering time:interacting pathways as a basis for diversity. Plant Cell. 2002, 14(Suppl.),S111–S130.
[2]Komeda, Y. Genetic regulation of time to flower in Arabidopsis thaliana. Annu.Rev. Plant Biol. 2004, 55, 521–535.
[3]Fornara, F., de Montaigu, A., and Coupland, G. (2010). SnapShot: control offlowering in Arabidopsis. Cell. 2010, 141, 550.
[4]Gibson J. L., Whipker B. E. Efficacy of plant growth regulators on the growthof vigorous Osteospermum cultivars. Hort Technology. 2003,13:132–135.
[5]Currey Christopher J, Erwin John E. Foliar Applications of Plant GrowthRegulators Affect Stem Elongation and Branching of 11 Kalanchoe Species. HortTechnolog. 2012, 22(3):338–344.
[6]Fu Y.F., Meng F.J. Flowering Physiological Signals in Plant. Journal of ChinaAgricultural University. 1998,3:1–11.
[7]Wang B.L., Zheng J.Y., Zeng G.W.. Changes in Carbohydrate Content of StemApices and Leaves during Floral Bud Differentiation in Radish (Raphanus sativusL.) Acta Horticulturae Sinica. 2004, 31:375– 377.
[8]Liu Y.T., Li C. Y., Shi X.X., Feng H., Wang Y.G. Identification of QTLs withadditive, epistatic, and QTL × environment interaction effects for the boltingtrait in Brassica rapa L. Euphytica. 2016, 210:427–439.
[9]Moe R. Effect of photoperiod and temperature on bolting in Chinese cabbage. Sci.Hortic..1985, 27:49–54.
[10]Yoshida, Y., Takada, N., and Koda, Y. Isolation and identification of ananti-bolting compound, hexadecatrienoic acid monoglyceride, responsible forinhibition of bolting and maintenance of the leaf rosette in radish plants.Plant Cell Physiol. 2010, 51, 1341–1349.
[11]Xiao, X., Lei, J., Cao, B., Chen, G., and Chen, C. cDNA-AFLP analysis onbolting or flowering of flowering Chinese cabbage and molecular characteristicsof BrcuDFR-like/BrcuAXS gene. Mol. Biol. Rep. 2012, 39, 7525–7531.
[12]Nie, S., Li, C., Xu, L., Wang, Y., Huang, D., Muleke, E. M., et al. De novotranscriptome analysis in radish (Raphanus sativus L.) and identification ofcritical genes involved in bolting and flowering. BMC Genomics. 2016, 17:389.
[13]Fukuda, M., Matsuo, S., Kikuchi, K., Mitsuhashi, W., Toyomasu, T., and Honda,I. (2009). The endogenous level of GA(1) is upregulated by high temperatureduring stem elongation in lettuce through LsGA3ox1 expression. Plant Physiol.2009, 166, 2077–2084.
[14]Han Y, Chen Z, Lv S, et al. MADS-Box Genes and Gibberellins Regulate Bolting inLettuce (Lactuca sativa L.). Front. Plant Sci. 2016, 7:1889.
[15]Liu X, Lv S, Ran L, et al. Transcriptomic analysis reveals the roles ofgibberellin-regulated genes and transcription factors in regulating bolting inlettuce (Lactuca sativa L.). Plos One, 2018, 13(2):e0191518.
[16]Chen Z, Zhao W, Ge D, et al. LCM-seq reveals the crucial role of LsSOC1 inheat-promoted bolting of lettuce (Lactuca sativa L.). Plant J., 2018; 95(3).
[17] LiuR, Su Z, Zhou H, et al. LsHSP70 is induced by high temperature to interact withcalmodulin, leading to higher bolting resistance in lettuce. Scientific Reports.2020, 10(1):15155.
[18]Chen Z, Han Y, Ning K, et al. Inflorescence Development and the Role of LsFT inRegulating Bolting in Lettuce (Lactuca sativa L.). Front. Plant Sci. 2017,8:2248-.
[19]Ning K, Han Y, et al. Genome-wide analysis of MADS-box family genes duringflower development in lettuce. Plant Cell Environ., 2019,42(6):1868-1881.
[20] Han R, Truco MJ,Lavelle DO, Michelmore RW. A Composite Analysis ofFlowering Time Regulation in Lettuce. Front Plant Sci. 2021,8;12:632708.

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