Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS

Rosas, Ulises; Mei, Yu; Xie, Qiguang; Banta, Joshua A.; Zhou, Royce W.; Seufferheld, Gabriela; Gerard, Silvia; Chou, Lucy; Bhambhra, Naeha; Parks, Jennifer Deane; Flowers, Jonathan M.; McClung, C. Robertson; Hanzawa, Yoshie; Purugganan, Michael D.

doi:10.1038/ncomms4651

Cited by 79 publications

(66 citation statements)

References 36 publications

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“…There is natural variation in the number of tandem repeats (two to four) of the DOF binding sites in the CO promoter among Arabidopsis wild-type accessions. When the number of DOF binding sites is higher, the daytime suppression of CO is greater and flowering time is consequently delayed more (Rosas et al, 2014). Temporal expression profiles of CDFs are directly controlled by the circadian clock (Nakamichi et al, , 2012Ito et al, 2008;Fornara et al, 2009).…”

Section: Temporal Transcriptional Regulation Of Comentioning

confidence: 99%

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

2016

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Plants sense changes in day length (= photoperiod) as a reliable seasonal cue to regulate important developmental transitions such as flowering. Integration of various external light information into the circadian clock-controlled mechanisms enables plants to precisely measure photoperiod changes in the surrounding environment. The core mechanism of photoperiodic measurement is regulation of CONSTANS (CO) activity, which takes place in phloem companion cells in leaves. Until recently, it remained unclear whether plants possess specific variations of the clock for this regulation. Now it is known that a specific circadian timing mechanism in the vascular tissue is essential for photoperiodic flowering. In addition to spatial tissue-specific regulation, temporal regulation of CO activity is also important. The identification and characterization of multiple regulators that physically interact with CO and influence its function in the morning in long days are two recent advances in photoperiodic regulation of flowering time. It seems that CO acts as a network hub to integrate various external and internal signals into the photoperiodic flowering pathway. CO regulates the amount of FLOWERING LOCUS T (FT) transcripts and FT protein moves from companion cells of leaf phloem to the shoot apical meristem. The protein that helps long-distance transport of FT protein was also identified recently. Here, we introduce recent advances in tissue-specific variations of the circadian clock and the emerging picture of the intricate connections of transcriptional regulators through CO in the morning, which all facilitate plants knowing when to flower.Properly timing the floral transition is crucial for reproductive success. It can also influence the early development of offspring. To optimize this timing, plants constantly monitor changes in the surrounding environment. Among various environmental factors, observing changes in day length (= photoperiod) is the most reliable way for many organisms to know the specific time of year. Therefore, photoperiodic regulation is one of the major flowering time mechanisms and it has been studied since it was first reported in 1920 (Song et al., 2015). Arabidopsis (Arabidopsis thaliana), as it flowers mainly in spring, can sense lengthening days to induce flowering and became a suitable model to study photoperiodic flowering regulation. (Andrés and Coupland, 2012;Song et al., 2013;Pajoro et al., 2014;Shim and Imaizumi, 2015).In principle, photoperiodic flowering mechanisms can be divided into three parts: light input, circadian clock, and output. Light information is integrated into innate photoperiodic timing mechanisms governed by the circadian clock to induce genes that trigger flowering.

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Section: Temporal Transcriptional Regulation Of Comentioning

confidence: 99%

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

2016

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“…Model organism studies have demonstrated significant functional consequences of even subtle unit number variation in select STRs in plants, fungi, flies, voles, dogs, and fish, among other organisms (Sawyer et al 1997;Fondon and Garner 2004;Hammock and Young 2005;Michael et al 2007;Undurraga et al 2012;Scarpino et al 2013;Rosas et al 2014). Similar to humans, STR-containing genes in these organisms tend to be regulatory genes functioning in transcription, development, and sensing environmental factors (Fondon and Garner 2004;Verstrepen et al 2005).…”

Section: [Supplemental Materials Is Available For This Article]mentioning

confidence: 99%

MIPSTR: a method for multiplex genotyping of germline and somatic STR variation across many individuals

et al. 2015

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Short tandem repeats (STRs) are highly mutable genetic elements that often reside in regulatory and coding DNA. The cumulative evidence of genetic studies on individual STRs suggests that STR variation profoundly affects phenotype and contributes to trait heritability. Despite recent advances in sequencing technology, STR variation has remained largely inaccessible across many individuals compared to single nucleotide variation or copy number variation. STR genotyping with short-read sequence data is confounded by (1) the difficulty of uniquely mapping short, low-complexity reads; and (2) the high rate of STR amplification stutter. Here, we present MIPSTR, a robust, scalable, and affordable method that addresses these challenges. MIPSTR uses targeted capture of STR loci by single-molecule Molecular Inversion Probes (smMIPs) and a unique mapping strategy. Targeted capture and our mapping strategy resolve the first challenge; the use of single molecule information resolves the second challenge. Unlike previous methods, MIPSTR is capable of distinguishing technical error due to amplification stutter from somatic STR mutations. In proof-of-principle experiments, we use MIPSTR to determine germline STR genotypes for 102 STR loci with high accuracy across diverse populations of the plant A. thaliana. We show that putatively functional STRs may be identified by deviation from predicted STR variation and by association with quantitative phenotypes. Using DNA mixing experiments and a mutant deficient in DNA repair, we demonstrate that MIPSTR can detect low-frequency somatic STR variants. MIPSTR is applicable to any organism with a high-quality reference genome and is scalable to genotyping many thousands of STR loci in thousands of individuals.

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“…Moreover, the phenotypic effects of ELF3 STR variants differed dramatically between the divergent backgrounds Col and Ws, consistent with the existence of background-specific modifiers. Genetic incompatibilities involving variation in several other STRs have been described in plants, flies, and fish (Peixoto et al 1998;Scarpino et al 2013;Rosas et al 2014). Taken together, these observations argue that STR variation underlies substantial phenotypic variation and may also underlie some genetic incompatibilities.…”

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confidence: 75%

The Conserved PFT1 Tandem Repeat Is Crucial for Proper Flowering in Arabidopsis thaliana

et al. 2014

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It is widely appreciated that short tandem repeat (STR) variation underlies substantial phenotypic variation in organisms. Some propose that the high mutation rates of STRs in functional genomic regions facilitate evolutionary adaptation. Despite their high mutation rate, some STRs show little to no variation in populations. One such STR occurs in the Arabidopsis thaliana gene PFT1 (MED25), where it encodes an interrupted polyglutamine tract. Although the PFT1 STR is large (270 bp), and thus expected to be extremely variable, it shows only minuscule variation across A. thaliana strains. We hypothesized that the PFT1 STR is under selective constraint, due to previously undescribed roles in PFT1 function. We investigated this hypothesis using plants expressing transgenic PFT1 constructs with either an endogenous STR or synthetic STRs of varying length. Transgenic plants carrying the endogenous PFT1 STR generally performed best in complementing a pft1 null mutant across adult PFT1-dependent traits. In stark contrast, transgenic plants carrying a PFT1 transgene lacking the STR phenocopied a pft1 loss-of-function mutant for flowering time phenotypes and were generally hypomorphic for other traits, establishing the functional importance of this domain. Transgenic plants carrying various synthetic constructs occupied the phenotypic space between wild-type and pft1 loss-of-function mutants. By varying PFT1 STR length, we discovered that PFT1 can act as either an activator or repressor of flowering in a photoperiod-dependent manner. We conclude that the PFT1 STR is constrained to its approximate wild-type length by its various functional requirements. Our study implies that there is strong selection on STRs not only to generate allelic diversity, but also to maintain certain lengths pursuant to optimal molecular function. SHORT tandem repeats (STRs, microsatellites) are ubiquitous and unstable genomic elements that have extremely high mutation rates (Subramanian et al. 2003;Legendre et al. 2007;Eckert and Hile 2009), leading to STR unit number variation within populations. STR variation in coding and regulatory regions can have significant phenotypic consequences (Gemayel et al. 2010). For example, several devastating human diseases, including Huntington's disease and spinocerebellar ataxias, are caused by expanded STR alleles (Hannan 2010). However, STR variation can also confer beneficial phenotypic variation and may facilitate adaptation to new environments (Fondon et al. 2008;Gemayel et al. 2010). For example, in Saccharomyces cerevisiae natural polyQ variation in the FLO1 protein underlies variation in flocculation, which is important for stress resistance and biofilm formation in yeasts (Verstrepen et al. 2005). Natural STR variants of the Arabidopsis thaliana gene ELF3, which encode variable polyQ tracts, can phenocopy elf3 loss-of-function phenotypes in a common reference background (Undurraga et al. 2012). Moreover, the phenotypic effects of ELF3 STR variants differed dramatically between the divergent ...

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Variation in Arabidopsis flowering time associated with cis-regulatory variation in CONSTANS

Cited by 79 publications

References 36 publications

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

MIPSTR: a method for multiplex genotyping of germline and somatic STR variation across many individuals

The Conserved PFT1 Tandem Repeat Is Crucial for Proper Flowering in Arabidopsis thaliana

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