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Molecular and Structural Characterization of Barley Vernalization Genes

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Molecular and Structural Characterization of Barley Vernalization Genes Plant Molecular Biology (2005) 59:449–467 Ó Springer 2005 DOI 10.1007/s11103-005-0351-2 Molecular and structural characterization of barley vernalization genes Jarislav von Zitzewitz1, ,Pe´ter Szucs} 1,3, , Jorge Dubcovsky4, Liuling Yan4, Enrico Francia5, Nicola Pecchioni6, Ana Casas7, Tony H.H. Chen2, Patrick M. Hayes1,* and Jeffrey S. Skinner1,2 1Department of Crop and Soil Science, Oregon State University, 253 Crop Science Building, Corvallis, OR 97331, USA (*author for correspondence; e-mail [email protected]); 2Department of Horticulture, Oregon State University, 4017 Ag. and Life Sci. Bldg., Corvallis, OR 97331-7304, USA; 3Agricultural Research Institute of the Hungarian Academy of Sciences, H-2462, Martonva´sa´r, Hungary; 4Department of Agronomy & Range Science, University of California, Davis, CA 95616, USA; 5Experimental Institute for Cereal Research, I)29017, Fiorenzuola d’Arda, PC Italy; 6Department of Agricultural Sciences, Universita` di Modena e Reggio Emilia, I)42100, Reggio Emilia, Italy; 7Aula Dei Experimental Station, CSIC, E)50059, Zaragoza, Spain; These authors contributed equally to this work Received 21 March 2005; accepted in revised form 28 June 2005 Key words: barley, HvBM5A, Triticeae, vernalization, VRN-H1, VRN-H2 Abstract Vernalization, the requirement of a period of low temperature to induce transition from the vegetative to reproductive state, is an evolutionarily and economically important trait in the Triticeae. The genetic basis of vernalization in cultivated barley (Hordeum vulgare subsp. vulgare) can be defined using the two-locus VRN-H1/VRN-H2 model. We analyzed the allelic characteristics of HvBM5A, the candidate gene for VRN-H1, from ten cultivated barley accessions and one wild progenitor accession (subsp. spontaneum), representing the three barley growth habits – winter, facultative, and spring. We present multiple lines of evidence, including sequence, linkage map location, and expression, that support HvBM5A being VRN-H1. While the predicted polypeptides from different growth habits are identical, spring accessions contain a deletion in the first intron of HvBM5A that may be important for regulation. While spring HvBM5A alleles are typified by the intron-localized deletion, in some cases, the promoter may also determine the allele type. The presence/absence of the tightly linked ZCCT-H gene family members on chromosome 4H perfectly correlates with growth habit and we conclude that one of the three ZCCT-H genes is VRN-H2. The VRN-H2 locus is present in winter genotypes and deleted from the facultative and spring genotypes analyzed in this study, suggesting the facultative growth habit (cold tolerant, vernalization unresponsive) is a result of deletion of the VRN-H2 locus and presence of a winter HvBM5A allele. All reported barley vernalization QTLs can be explained by the two-locus VRN-H1/VRN-H2 model based on the presence/ absence of VRN-H2 and a winter vs. spring HvBM5A allele. Abbreviations: gDNA, genomic DNA; InDel, insertion/deletion; LD, long day; MITE, miniature inverted- repeat transposable element; QTL, quantitative trait locus; RT-PCR, reverse transcription polymerase chain reaction; SD, short day; SNP, single nucleotide polymorphism; SSR, simple sequence repeat; UTR, untranslated region; VRN, vernalization 450 Introduction cloning of candidate genes in diploid wheat (Triticum monococcum) for VRN-Am1 and VRN- Vernalization – the induction of flowering by Am2 (Yan et al., 2003, 2004a) and hexaploid wheat exposure to an extended period of low temperature (T. aestivum) for VRN-1 (Danyluk et al., 2003; – is characteristic of many temperate zone plants, Trevaskis et al., 2003) has considerably advanced including ‘winter growth habit’ forms of the our understanding of vernalization in the econom- Triticeae. Vernalization requirement is of particu- ically important cereals. lar interest in the cereal crops due to its role in Takahashi and Yasuda (1971) proposed a determining adaptation range and association with three-locus epistatic model for barley vernalization winter hardiness, i.e., the capacity of a genotype to requirement where winter growth habit genotypes survive the winter (Hayes et al., 1997). The prin- have the allelic architecture Sh_sh2sh2sh3sh3; all cipal components of cereal winter hardiness are other allelic configurations lack vernalization low temperature tolerance, vernalization require- requirement and yield the spring and facultative ment, and photoperiod (day length) sensitivity. growth habits. Based on wheat:barley orthology, Relative to these trait combinations, the barley we use the standard Triticeae nomenclature, with (Hordeum vulgare subsp. vulgare) germplasm can an ‘‘H’’ to indicate the Hordeum genome: be divided into two broad winter hardiness growth Sh2=VRN-H1 (chromosome 5H); Sh=VRN-H2 habit classifications – winter and spring. In gen- (chromosome 4H); and Sh3 = VRN-H3 (chromo- eral, winter varieties are low temperature tolerant, some 1H), in the remainder of this report. Allelic photoperiod sensitive, and vernalization requiring; variants at the VRN-H3 locus are reported only in while we use the term ‘requirement’ for standard- exotic barley genotypes (Takahashi and Yasuda, ization with other cereal nomenclature, winter 1971), reducing the epistatic model to a two-locus barley varieties are actually strongly vernalization (VRN-H2 and VRN-H1) model in cultivated responsive rather than requiring, as they will barley. flower, eventually, without vernalization (Karsai A molecular model explaining the VRN-2/ et al., 2001). In contrast, spring varieties are VRN-1 epistatic interaction in the Triticeae was essentially the opposite and have minimal low proposed by Yan et al. (2004a) based on the temperature tolerance capacity, do not require positional cloning of VRN-Am1 and VRN-Am2 in vernalization, and are typically insensitive to short T. monococcum, in which VRN-Am2 encodes a day photoperiod. A third growth habit class – dominant repressor of flowering (ZCCT1) which facultative – occurs in the barley germplasm which inhibits the expression of the VRN-Am1 flowering represents a subclass of the winter growth habit. gene TmAP1 (T. monococcum AP1). Vernalization The facultative growth habit lacks an unambigu- down-regulates Vrn-Am2 (ZCCT1) expression, ous definition, but is typically utilized to refer to allowing expression of vrn-Am1 in winter genotypes that are as low temperature tolerant as accessions, while no vernalization requirement is winter varieties, but lack a vernalization require- observed in accessions with a physical deletion of ment. the ZCCT genes (vrn-Am2 locus), regardless of the The genetics of vernalization in Arabidopsis is allele at VRN-Am1, as well as in genotypes that well-characterized (see review by Henderson et al., have Vrn-Am2 but lack a target binding site for the 2003). While Triticeae vernalization genetics is not repressor in the TmAP1 gene (i.e., dominant as complete, it appears that a different pathway Vrn-Am1). A deletion in the promoter region of leads to the same end phenotype relative to VRN-Am1 that correlated with spring vs. winter Arabidopsis (Takahashi and Yasuda, 1971; Karsai growth habit was proposed as a possible et al., 2001; Danyluk et al., 2003; Trevaskis et al., VRN-Am2 target site (Yan et al., 2003). In sub- 2003; Yan et al., 2003, 2004a; Cooper et al., 2005). sequent work, we determined that in some spring The Triticeae form a homogeneous genetic system wheat accessions, the promoter is invariant relative with a high degree of synteny in which the genetic to winter accessions (Yan et al., 2004b). This determinants of winter hardiness are conserved, suggests additional regulatory sites may be located and results of one species are frequently applicable intragenically, and that in wheat, VRN-1 response to other members of the cereal tribe (Dubcovsky to vernalization can be controlled either from the et al., 1998; Mahfoozi et al., 2000). The recent promoter and/or intragenically. In the remainder 451 of this work, we use the generic terms ‘spring growth habits follows the predicted pattern based allele’ to refer to alleles for the deleted VRN-2 on the VRN-H1 and VRN-H2 alleles combinations locus (recessive vrn-2 allele) and the un-repressible that are present, (iii) growth habit correlates with Vrn-1 allele and ‘winter allele’ to refer to alleles the presence/absence of VRN-H2 in the same encoding the functional repressor of the VRN-2 germplasm array, and (iv) allelic variation at the locus (dominant Vrn-2 allele) and the repressible VRN-H loci explains QTL mapping results. vrn-1 allele. HvBM5, the barley ortholog of TmAP1 (VRN-Am1) (Yan et al., 2003), was cloned during a MADS-box screen by Schmitz et al. Materials and methods (2000) and its orthology with TaVRT-1 (VRN-B1) and WAP1 (VRN-D1) has been established; Plant material and growth conditions TaVRT-1 (Danyluk et al. 2003) and WAP1 (Murai et al., 1998; Trevaskis et al. 2003) repre- Ten Hordeum vulgare subsp. vulgare genotypes, sent AP1 homoeologs from hexaploid wheat. representing both the three barley growth habit Prior to the cloning of candidate genes, quanti- phenotype classes and parents from six primary tative trait locus (QTL) analysis tools were em- barley winter hardiness QTL mapping popula- ployed to dissect vernalization genetic traits in the tions, were utilized for allelic studies. These are (i) Triticeae, which was simplified by the use of diploid four winter habit genotypes: Kompolti korai, barley and doubled haploid progeny. For
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