The Role of a Pseudo-Response Regulator Gene in Life Cycle Adaptation and Domestication of Beet

Abstract

Life cycle adaptation to latitudinal and seasonal variation in photoperiod and temperature is a major determinant of evolutionary success in flowering plants. Whereas the life cycle of the dicotyledonous model species Arabidopsis thaliana is controlled by two epistatic genes, FLOWERING LOCUS C and FRIGIDA, three unrelated loci (VERNALIZATION) determine the spring and winter habits of monocotyledonous plants such as temperate cereals. In the core eudicot species Beta vulgaris, whose lineage diverged from that leading to Arabidopsis shortly after the monocot-dicot split 140 million years ago, the bolting locus B is a master switch distinguishing annuals from biennials. Here, we isolated B and show that the pseudo-response regulator gene BOLTING TIME CONTROL 1 (BvBTC1), through regulation of the FLOWERING LOCUS T genes, is absolutely necessary for flowering and mediates the response to both long days and vernalization. Our results suggest that domestication of beets involved the selection of a rare partial loss-of-function BvBTC1 allele that imparts reduced sensitivity to photoperiod that is restored by vernalization, thus conferring bienniality, and illustrate how evolutionary plasticity at a key regulatory point can enable new life cycle strategies.

The genome of the recently domesticated crop plant sugar beet (Beta vulgaris)

“…These regions may represent traces of breeding activities which aimed at introducing sea beet traits into sugar beet. The gene BvBTC1, encoded by the B-locus 16 and located in a 1.1 Mb RefBeet scaffold on chromosome 2, plays an important role during vernalization. Cultivated lines are homozygotes for the B allele resulting in a biennial life cycle.…”

Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon

“…Dominant alleles of BvBTC1 result in an annual habit, whereas recessive alleles (Bvbtc1) confer a vernalization requirement and biennial growth habit. BvBTC1 encodes a pseudoresponse regulator with homology to the Arabidopsis PSEUDORESPONSE REGULATOR3 (PRR3) and PRR7 and barley (Hordeum vulgare) PHOTOPERIOD1-H1 genes (Pin et al, 2012). Dominant BvBTC1 alleles in annual sugar beets are associated with low mRNA levels of BvFT1, a repressor within the FT subfamily, and high mRNA levels of the Arabidopsis FT ortholog, BvFT2, and this is associated with rapid flowering without vernalization.…”

“…Dominant BvBTC1 alleles in annual sugar beets are associated with low mRNA levels of BvFT1, a repressor within the FT subfamily, and high mRNA levels of the Arabidopsis FT ortholog, BvFT2, and this is associated with rapid flowering without vernalization. In nonvernalized plants, which are delayed in flowering, recessive Bvbtc1 alleles are associated with high mRNA levels of BvFT1 and low mRNA levels of BvFT2 (Pin et al, 2012). BvFT1 is hypothesized to act upstream of BvFT2 because overexpression of BvFT1 results in lower level of BvFT2 mRNA (Pin et al, 2010).…”

“…BvFT1 is hypothesized to act upstream of BvFT2 because overexpression of BvFT1 results in lower level of BvFT2 mRNA (Pin et al, 2010). During cold in biennial beet, Bvbtc1 expression increases and BvFT1 expression decreases, permitting high BvFT2 expression in subsequent long days of spring to promote flowering (Pin et al, 2010(Pin et al, , 2012.…”

Genetic and Epigenetic Mechanisms Underlying Vernalization

“…Vernalization-induced repression of BvFT1 is stably maintained even after plants are returned to warm growth temperatures, indicating that BvFT1 functions similarly to FLC. Vernalization requirement in sugar beet is mainly conferred by a dominant allele named BvBTC1 through its regulation of BvFT1 and BvFT2 (Pin et al, 2012) …”