Regulation of Temperature-Responsive Flowering by MADS-Box Transcription Factor Repressors

Lee, Jeong‐Hwan; Ryu, Hak Seung; Chung, Kwansoo; Posé, David; Kim, Soonkap; Schmid, Markus; Ahn, Ji Hoon

doi:10.1126/science.1241097

Cited by 319 publications

(426 citation statements)

References 56 publications

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“…This short haplotype block spans a single gene, AGAMOUS-LIKE 50 (AGL50), which encodes a MADSbox transcription factor. Many other members of the MADS-box family play critical roles in flowering time control (58)(59)(60), but the functions of AGL50 and its closest paralog AGL49, which belong to a poorly characterized clade of the MADS-box family (61) (Fig. 4B), we sequenced the coding region of AGL50 from each of the 30 parental accessions (SI Appendix, Fig.…”

Section: Resultsmentioning

confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The ubiquity of nonparental hybrid phenotypes, such as hybrid vigor and hybrid inferiority, has interested biologists for over a century and is of considerable agricultural importance. Although examples of both phenomena have been subject to intense investigation, no general model for the molecular basis of nonadditive genetic variance has emerged, and prediction of hybrid phenotypes from parental information continues to be a challenge. Here we explore the genetics of hybrid phenotype in 435 Arabidopsis thaliana individuals derived from intercrosses of 30 parents in a half diallel mating scheme. We find that nonadditive genetic effects are a major component of genetic variation in this population and that the genetic basis of hybrid phenotype can be mapped using genome-wide association (GWA) techniques. Significant loci together can explain as much as 20% of phenotypic variation in the surveyed population and include examples that have both classical dominant and overdominant effects. One candidate region inherited dominantly in the half diallel contains the gene for the MADS-box transcription factor AGAMOUS-LIKE 50 (AGL50), which we show directly to alter flowering time in the predicted manner. Our study not only illustrates the promise of GWA approaches to dissect the genetic architecture underpinning hybrid performance but also demonstrates the contribution of classical dominance to genetic variance.T he often observed phenotypic superiority of progeny relative to their parents, or heterosis, is a universal phenomenon and of great importance to plant agriculture. The earliest description of heterosis (also known as hybrid vigor or superiority) dates to Darwin's studies of cross-fertilization in plants. He noticed that intercrossing distantly related individuals gave rise to larger, more vigorous progeny (1). Four decades later, George Shull coined the term "heterosis" (2) for this phenomenon, which he and Edward East had independently described for hybrids of inbred maize in 1908 (3, 4). Heterosis has long been of interest to evolutionary biologists as a potential explanation for the ubiquity of cross-fertilization in plants and animals, but it is also a central component of agricultural breeding programs. The combination of hybrid seed technology and inbred line improvement has driven an unprecedented improvement in maize yield over the past century (5). Despite the economic importance of heterosis and its intensive investigation in a wide spectrum of species, prediction of hybrid performance from parental information remains a major challenge (6).In the terms of quantitative genetics, hybrid vigor (and its opposite, inferiority) describes a deviation of progeny from the phenotypic mean of the parents. This means that heterosis cannot be explained by the addition of the effects of contributing alleles (7). Nonadditive genetic variance can result from a nonlinear phenotypic effect of alleles at one locus, as in the case of dominant/recessive allele pairs in classical genetics, or from epistatic interactions ...

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Section: Resultsmentioning

confidence: 99%

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seymour

Chae

Grimm

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…For example, SVP complexes with FLOWERING LOCUS C (FLC) to permit flowering only once FLC levels are sufficiently reduced by progressive chromatin changes in response to prolonged vernalization (Michaels and Amasino, 1999;Bastow et al, 2004;Sung and Amasino, 2004;Li et al, 2008). In addition, repressive complexes of SVP with FLOWERING LOCUS M or MADS AFFECTING FLOWERING2 decline at warmer temperatures, contributing to thermoresponsive flowering (Ratcliffe et al, 2003;Gu et al, 2013;Lee et al, 2013;Posé et al, 2013;Airoldi et al, 2015;Sureshkumar et al, 2016).…”

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confidence: 99%

Seasonal Regulation of Petal Number

et al. 2017

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Four petals characterize the flowers of most species in the Brassicaceae family, and this phenotype is generally robust to genetic and environmental variation. A variable petal number distinguishes the flowers of Cardamine hirsuta from those of its close relative Arabidopsis (Arabidopsis thaliana), and allelic variation at many loci contribute to this trait. However, it is less clear whether C. hirsuta petal number varies in response to seasonal changes in environment. To address this question, we assessed whether petal number responds to a suite of environmental and endogenous cues that regulate flowering time in C. hirsuta. We found that petal number showed seasonal variation in C. hirsuta, such that spring flowering plants developed more petals than those flowering in summer. Conditions associated with spring flowering, including cool ambient temperature, short photoperiod, and vernalization, all increased petal number in C. hirsuta. Cool temperature caused the strongest increase in petal number and lengthened the time interval over which floral meristems matured. We performed live imaging of early flower development and showed that floral buds developed more slowly at 15°C versus 20°C. This extended phase of floral meristem formation, coupled with slower growth of sepals at 15°C, produced larger intersepal regions with more space available for petal initiation. In summary, the growth and maturation of floral buds is associated with variable petal number in C. hirsuta and responds to seasonal changes in ambient temperature.

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“…Temperature-dependent differences in flowering time are controlled by multiple factors that mainly affect the expression levels of one of the key floral activators, the FLOWERING LOCUS T (FT) gene (Kardailsky et al, 1999;Kobayashi et al, 1999). Low ambient temperatures reduce the expression of FT, although this decrease is not caused by changes in its transcriptional activator CONSTANS (CO), which reveals the importance of floral repressors controlling flowering time under low ambient temperatures (16°C; Blázquez et al, 2003;Lee et al, 2013). However, the levels of TWIN SISTER OF FLOWERING LOCUS T (TSF), the closest homolog of FT, are similar at both temperatures, resulting in a higher expression of TSF than FT at 16°C (Blázquez et al, 2003;Lee et al, 2012Lee et al, , 2013.…”

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confidence: 99%

SHORT VEGETATIVE PHASE Up-Regulates TEMPRANILLO2 Floral Repressor at Low Ambient Temperatures

et al. 2015

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Plants integrate day length and ambient temperature to determine the optimal timing for developmental transitions. In Arabidopsis (Arabidopsis thaliana), the floral integrator FLOWERING LOCUS T (FT) and its closest homolog TWIN SISTER OF FT promote flowering in response to their activator CONSTANS under long-day inductive conditions. Low ambient temperature (16°C) delays flowering, even under inductive photoperiods, through repression of FT, revealing the importance of floral repressors acting at low temperatures. Previously, we have reported that the floral repressors TEMPRANILLO (TEM; TEM1 and TEM2) control flowering time through direct regulation of FT at 22°C. Here, we show that tem mutants are less sensitive than the wild type to changes in ambient growth temperature, indicating that TEM genes may play a role in floral repression at 16°C. Moreover, we have found that TEM2 directly represses the expression of FT and TWIN SISTER OF FT at 16°C. In addition, the floral repressor SHORT VEGETATIVE PHASE (SVP) directly regulates TEM2 but not TEM1 expression at 16°C. Flowering time analyses of svp tem mutants indicate that TEM may act in the same genetic pathway as SVP to repress flowering at 22°C but that SVP and TEM are partially independent at 16°C. Thus, TEM2 partially mediates the temperature-dependent function of SVP at low temperatures. Taken together, our results indicate that TEM genes are also able to repress flowering at low ambient temperatures under inductive long-day conditions. Plants constantly monitor environmental and endogenous signals to control their growth and adjust developmental responses to daily and seasonal cues (Penfield, 2008). During the juvenile phase, plants are not competent to flower; they are insensitive to inductive environmental factors, such as favorable conditions of day length or temperature. The transition to the adult phase permits reaching the competence to respond to those signals, which is essential to trigger flowering during the reproductive phase (Bergonzi and Albani, 2011;Huijser and Schmid, 2011). Consequently, the control of flowering time is a key determinant of reproductive success and plays an essential role in plant adaptation to seasons and geography.Flowering time is controlled by an intricate network of interdependent genetic pathways that monitor and respond to both endogenous and environmental signals. These pathways include age, photoperiod and light quality, GA, thermosensory (ambient temperature), vernalization, and autonomous pathways (Fornara et al., 2010;Srikanth and Schmid, 2011). In Arabidopsis (Arabidopsis thaliana), it is well documented the noteworthy regulation of the timing of flowering by day length or photoperiod and temperature (for review, see Andrés and Coupland, 2012;Song et al., 2013;Chew et al., 2014;Romera-Branchat * Address correspondence to soraya.pelaz@cragenomica.es. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions f...

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Regulation of Temperature-Responsive Flowering by MADS-Box Transcription Factor Repressors

Cited by 319 publications

References 56 publications

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Genetic architecture of nonadditive inheritance inArabidopsis thalianahybrids

Seasonal Regulation of Petal Number

SHORT VEGETATIVE PHASE Up-Regulates TEMPRANILLO2 Floral Repressor at Low Ambient Temperatures

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