Genome Dynamics Explain the Evolution of Flowering Time CCT Domain Gene Families in the Poaceae

Cockram, James; Thiel, Thomas; Steuernagel, Burkhard; Stein, Nils; Taudien, Stefan; Bailey, Paul; O’Sullivan, Donal M.

doi:10.1371/journal.pone.0045307

Cited by 100 publications

(159 citation statements)

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“…Another QTL is also found on chromosome 11 (at 2.78–2.79 Mb), between two candidate genes, Os11g05930 (encoding a response regulator receiver domain-containing protein) and Os11g05935 (encoding a mucin-type membrane protein involved in signal transduction). Note that Os11g05930 is the orthologue to HvPRR59 in barley, which has been associated with its early flowering time2930, while Os11g05935 has an orthologue in Caragana jubata 31, which was found to respond to cold stress. These two salinity tolerance loci are the first evidence of this type of loci on chromosome 11 (ref.…”

Section: Resultsmentioning

confidence: 99%

Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping

et al. 2016

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High-throughput phenotyping produces multiple measurements over time, which require new methods of analyses that are flexible in their quantification of plant growth and transpiration, yet are computationally economic. Here we develop such analyses and apply this to a rice population genotyped with a 700k SNP high-density array. Two rice diversity panels, indica and aus, containing a total of 553 genotypes, are phenotyped in waterlogged conditions. Using cubic smoothing splines to estimate plant growth and transpiration, we identify four time intervals that characterize the early responses of rice to salinity. Relative growth rate, transpiration rate and transpiration use efficiency (TUE) are analysed using a new association model that takes into account the interaction between treatment (control and salt) and genetic marker. This model allows the identification of previously undetected loci affecting TUE on chromosome 11, providing insights into the early responses of rice to salinity, in particular into the effects of salinity on plant growth and transpiration.

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Section: Resultsmentioning

confidence: 99%

Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping

et al. 2016

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“…Evolutionary History of Pooid VRN2/Ghd7 and CO9 Genes Two hypotheses about the evolutionary history of VRN2-like genes have been previously proposed (Cockram et al, 2012;Ream et al, 2012). One posits a single gene duplication event before the base of grasses, giving rise to a VRN2/Ghd7-and a CO9-containing clade and implying an orthologous relationship between pooid VRN2 genes and rice Ghd7 (Ream et al, 2012).…”

Section: Discussionmentioning

confidence: 99%

“…One posits a single gene duplication event before the base of grasses, giving rise to a VRN2/Ghd7-and a CO9-containing clade and implying an orthologous relationship between pooid VRN2 genes and rice Ghd7 (Ream et al, 2012). The other postulates two duplication events before the base of grasses, with the first giving rise to the VRN2 and Ghd7/CO9 clades and the second producing the Ghd7 and CO9 clades, followed by loss of Ghd7 genes at the base of pooids (Cockram et al, 2012). Our phylogenetic results based on VRN2/Ghd7/CO9-like sequences from multiple grass and other monocot species indicate that VRN2 is orthologous to rice Ghd7, supporting a single duplication event before the base of grasses that gave rise to Ghd7/VRN2 and CO9 clade genes.…”

Section: Discussionmentioning

confidence: 99%

Evolution of VRN2/Ghd7-Like Genes in Vernalization-Mediated Repression of Grass Flowering

et al. 2016

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Flowering of many plant species is coordinated with seasonal environmental cues such as temperature and photoperiod. Vernalization provides competence to flower after prolonged cold exposure, and a vernalization requirement prevents flowering from occurring prior to winter. In winter wheat (Triticum aestivum) and barley (Hordeum vulgare), three genes VRN1, VRN2, and FT form a regulatory loop that regulates the initiation of flowering. Prior to cold exposure, VRN2 represses FT. During cold, VRN1 expression increases, resulting in the repression of VRN2, which in turn allows activation of FT during long days to induce flowering. Here, we test whether the circuitry of this regulatory loop is conserved across Pooideae, consistent with their niche transition from the tropics to the temperate zone. Our phylogenetic analyses of VRN2-like genes reveal a duplication event occurred before the diversification of the grasses that gave rise to a CO9 and VRN2/Ghd7 clade and support orthology between wheat/barley VRN2 and rice (Oryza sativa) Ghd7. Our Brachypodium distachyon VRN1 and VRN2 knockdown and overexpression experiments demonstrate functional conservation of grass VRN1 and VRN2 in the promotion and repression of flowering, respectively. However, expression analyses in a range of pooids demonstrate that the cold repression of VRN2 is unique to core Pooideae such as wheat and barley. Furthermore, VRN1 knockdown in B. distachyon demonstrates that the VRN1-mediated suppression of VRN2 is not conserved. Thus, the VRN1-VRN2 feature of the regulatory loop appears to have evolved late in the diversification of temperate grasses.The initiation of flowering is a major developmental transition in the plant life cycle. When flowering initiates, shoot apical meristems shift from forming vegetative organs such as leaves to forming flowers. In many plant species, flowering occurs at a particular time of year in response to the sensing of seasonal cues such as changes in day length and temperature. In some plants adapted to temperate climates, exposure to the prolonged cold of winter (vernalization) results in the ability to flower in the next growing season (Chouard, 1960;Amasino, 2010). Although vernalization ultimately enables flowering, vernalization responsiveness is typically an adaptation to ensure that flowering does not occur prematurely in the fall season. This has obvious adaptive value; for example, many vernalization-responsive plants become established in the fall season (during which flowering would not lead to successful reproduction) and then rapidly flower in the spring when conditions for reproduction and seed maturation are optimal.The grass family (Poaceae) originated approximately 70 million years ago as part of the tropical forest understory. However, grasses have since diversified across the globe occupying a variety of ecological niches (Kellogg, 2001). Exemplifying this, the ;3,800 species of grass subfamily Pooideae, including the economically important cereals wheat (Triticum aestivum, Triticeae), barley (...

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“…Ghd7 belongs to the CCT motif family subclass of the CCT gene family with only a single CCT domain (Cockram et al, 2012). Ghd7 is up-regulated under LD conditions and represses Hd3a and flowering time.…”

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confidence: 99%

CONSTANS Controls Floral Repression by Up-Regulating VERNALIZATION2 (VRN-H2) in Barley

Mulki

Korff

2015

Plant Physiol.

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In barley (Hordeum vulgare), PHOTOPERIOD1 (Ppd-H1) acts as a major positive regulator of flowering under long-day conditions, while VERNALIZATION2 (VRN-H2) is a strong repressor of flowering under long days before vernalization. By contrast, CONSTANS (CO) plays a key role in the photoperiodic regulation of flowering in Arabidopsis (Arabidopsis thaliana). Here, we study the role of the closest barley CO homologs, HvCO1 and HvCO2, in the long day-dependent control of flowering and their interactions with Ppd-H1 and VRN-H2. HvCO2 overexpression in spring barley, with a natural deletion of the VRN-H2 locus, caused a Ppd-H1-dependent induction of flowering and FLOWERING LOCUS T1 (HvFT1) expression. In winter barley, which carries the VRN-H2 locus, overexpression of HvCO1/CO2 caused an up-regulation of VRN-H2, resulting in a reduced expression of HvFT1 and delayed flowering under long-and short-day conditions. In addition, natural variation at Ppd-H1 altered the expression of VRN-H2 in wild-type plants under long days. VRN-H2, in turn, was involved in the down-regulation of Ppd-H1 and HvCO2, demonstrating strong reciprocal interactions between HvCO2, Ppd-H1, and VRN-H2. Consequently, this study showed that the induction of the floral repressor VRN-H2 and the floral activator HvFT1 was regulated by the same genes, Ppd-H1 and HvCO1/CO2. Our findings provide a novel insight into the photoperiodic regulation of the vernalization pathway in barley.Flowering is one of the most critical stages in the life cycle of plants. The coincidence of flowering with favorable conditions ensures that seed production is maximized and enhances the chances of successful reproduction. A key adaptive mechanism to achieve this coincidence is sensing changes in daylength or photoperiod (Greenup et al., 2009). Long photoperiods promote flowering in the model and facultative long-day (LD) plant Arabidopsis (Arabidopsis thaliana) through the activity of CONSTANS (CO), a transcription factor that binds to the promotor of FLOWERING LOCUS T (FT), which, in turn, induces the floral transition (Putterill et al., 1995;Tiwari et al., 2010). CO encodes a protein with two zinc finger B-boxes and a CCT (CONSTANS, CONSTANS-like, and TIMING OF CAB EXPRESSION1 [TOC1]) domain (Robson et al., 2001). CO transcription is regulated by the circadian clock and its components in a way that allows the accumulation of CO mRNA at the end of the light period of long days (LDs) but after dusk in short days (SDs; Imaizumi et al., 2005;Fornara et al., 2009). The CO protein is stabilized by photoreceptors in the light and degraded by the ubiquitin ligase CONSTITUTIVE PHOTOMORPHO-GENIC1 during the dark, which allows the accumulation of CO at the end of a long day to induce FT transcription (Jang et al., 2008;Turck et al., 2008).The function of CO in controlling the photoperiod response is conserved in the short-day (SD) cereal monocot rice (Oryza sativa). Under inductive SDs, Heading date1 (Hd1), the rice ortholog of CO, promotes flowering by inducing the expression of Hd3a, ...

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Genome Dynamics Explain the Evolution of Flowering Time CCT Domain Gene Families in the Poaceae

Cited by 100 publications

References 73 publications

Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping

Salinity tolerance loci revealed in rice using high-throughput non-invasive phenotyping

Evolution of VRN2/Ghd7-Like Genes in Vernalization-Mediated Repression of Grass Flowering

CONSTANS Controls Floral Repression by Up-Regulating VERNALIZATION2 (VRN-H2) in Barley

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