Vernalization and Floral Transition in Autumn Drive Winter Annual Life History in Oilseed Rape

Abstract

SummaryPlants with winter annual life history germinate in summer or autumn and require a period of prolonged winter cold to initiate flowering, known as vernalization. In the Brassicaceae, the requirement for vernalization is conferred by high expression of orthologs of the FLOWERING LOCUS C (FLC) gene, the expression of which is known to be silenced by prolonged exposure to winter-like temperatures [1]. Based on a wealth of vernalization experiments, typically carried out in the range of 5°C–10°C, we would expect field environments during winter to induce flowering in crops with winter annual life history. Here, we show that, in the case of winter oilseed rape, expression of multiple FLC orthologs declines not during winter but predominantly during October when the average air temperature is 10°C–15°C. We further demonstrate that plants proceed through the floral transition in early November and overwinter as inflorescence meristems, which complete floral development in spring. To validate the importance of pre-winter temperatures in flowering time control, we artificially simulated climate warming in field trial plots in October. We found that increasing the temperature by 5°C in October results in raised FLC expression and delays the floral transition by 3 weeks but only has a mild effect on flowering date the following spring. Our work shows that winter annuals overwinter as a floral bud in a manner that resembles perennials and highlights the importance of studying signaling events in the field for understanding how plants transition to flowering under real environmental conditions.

The transition to flowering in winter rapeseed during vernalization

“…The development of floral buds in mid‐November and opening of the flowers in late April of the following year implied an active apical growth period in autumn that was followed by a cessation of growth in winter, leading to an extreme delay in floral buds' emergence and further flower development. Floral transition in autumn and overwintering of floral buds was also reported for other winter rapeseed cultivars grown in the UK (O'Neill et al, 2019). Since rapeseed floral buds are not encased by layers of bud scales like dormant tree buds, autumn‐driven vernalization might jeopardize the whole reproductive cycle of rapeseed plants, as the floral structures have to acquire winter hardiness to survive cold winters.…”

“…Interestingly, genes involved in ethylene biosynthesis and signalling were found to be in genomic regions with a strong selective‐sweep between winter and spring types (Wu et al, 2019). In consistence with the later flowering being associated with higher yield, recently, it has been shown that warmer temperatures in October, which lead to later floral induction in winter rapeseed, were associated with higher yields (Brown, Beeby, & Penfield, 2019; O'Neill et al, 2019). Therefore, more emphasis on the cold duration required for floral transition in different cultivars might identify genetic loci associated with longer vegetative growth and finally higher yields.…”

Step-wise increases inFT1expression regulate seasonal progression of flowering in wheat (Triticum aestivumL.)

“…The results highlight the importance of complementing laboratory-based analysis with experiments performed in the field -a concept echoed by work performed in oilseed rape, Arabidopsis and rice that have used field-grown plants to uncover new information about the molecular events controlling seasonal regulation of flowering (Duncan et al, 2015;Gomez-Ariza et al, 2015;Hepworth et al, 2018;Song et al, 2018;O'Neill et al, 2019). Our work provides an important foundation for understanding the mechanisms controlling yield-related traits of wheat, which is vital given our increasing need to improve global food security by generating superior yielding cultivars (Fischer et al, 2014).…”

Gene regulatory networks controlled by FLOWERING LOCUS C that confer variation in seasonal flowering and life history

“…Stable repression of FLC transcription in annuals allows plants to flower independently of age through the FT pathway after vernalization, whereas reactivation of FLC orthologues in perennials blocks FT transcription, which forces these plants to flower through the age-dependent SPL15 pathway. Recently, winter varieties of Brassica napus that flower in response to vernalization were found to produce flower buds in late autumn and open flowers in spring ( O’ Neill et al , 2019 ). In these plants, floral induction occurs under vernalizing conditions in autumn when the photoperiodic pathway is not expected to be active, and therefore might initiate flowering via the miR156/SPL15 pathway.…”