Autophagy regulated by day length determines the number of fertile florets in wheat

Abstract

SummaryThe wheat spikelet meristem differentiates into up to 12 floret primordia, but many of them fail to reach the fertile floret stage at anthesis. We combined microarray, biochemical and anatomical studies to investigate floret development in wheat plants grown in the field under short or long days (short days extended with lowfluence light) after all the spikelets had already differentiated. Long days accelerated spike and floret development and greening, and the expression of genes involved in photosynthesis, photoprotection and carbohydrate metabolism. These changes started while the spike was in the light-depleted environment created by the surrounding leaf sheaths. Cell division ceased in the tissues of distal florets, which interrupted their normal developmental progression and initiated autophagy, thus decreasing the number of fertile florets at anthesis. A massive decrease in the expression of genes involved in cell proliferation, a decrease in soluble carbohydrate levels, and an increase in the expression of genes involved in programmed cell death accompanied anatomical signs of cell death, and these effects were stronger under long days. We propose a model in which developmentally generated sugar starvation triggers floret autophagy, and long days intensify these processes due to the increased carbohydrate consumption caused by the accelerated plant development.

More fertile florets and grains per spike can be achieved at higher temperature in wheat lines with high spike biomass and sugar content at booting

“…This response is different to that observed for long photoperiods in sensitive lines, where accelerated growth and sugar depletion are the suggested cause for autophagy (e.g. Ghiglione et al 2008). However, it fits the description of a quantitative response to temperature with an optimum.…”

“…This study highlighted the link between the success of wheat reproductive structures in response to temperature utilising genotypic variation in water soluble carbohydrate metabolism, going beyond the evidence obtained by shading/light addition (Stockman et al 1983) and daylength manipulation and sucrose feeding (Ghiglione et al 2008). The corollary of the differential spike biomass, lower relative floret development rate till booting, together with the coordination of sucrose production, transport and cleavage was a higher number of fertile florets per spike under higher temperature and longer photoperiod for the High WSC lines.…”

“…the majority of floret development takes place), wheat floret fertility has been positively associated to (i) their developmental and anatomical status at the beginning of the period of rapid biomass accumulation of the spike (González et al 2005) and (ii) increased sugar concentration in the growing spike (Ghiglione et al 2008) or spike weight at anthesis (Miralles et al 2000;Gonzalez et al 2011). The idea that floret death is a process triggered by the stage of development of the most advanced floret in the spike has also been proposed (Bancal 2008(Bancal , 2009).…”

“…Long days after terminal spikelet accelerated the rate of floret development, brought forward the maximum growth rate of the spike and resulted in a reduced number of fertile florets per spikelet at anthesis (González et al 2005). Ghiglione et al (2008) proposed that the acceleration of spike growth under long days led to depletion of the spike carbohydrate pool and floral programmed cell death by autophagy. Dougherty et al (1975) and Fischer and Stockman (1980) have shown that increased levels of water soluble carbohydrates (WSC) in the spike were concurrent with higher grain number per spikelet and per spike in crops responding to shading, thinning, irrigation and fertilisation.…”

Global Transcriptome Profiling of Developing Leaf and Shoot Apices Reveals Distinct Genetic and Environmental Control of Floral Transition and Inflorescence Development in Barley

“…In contrast to vernalization, variations in photoperiod have minor effects on the duration of the vegetative phase but strongly accelerate the early and late reproductive phases of inflorescence development in wheat and barley Slafer et al, 2001). The duration of the spike growth phase has been identified as a major determinant of seed number (Fischer, 1985;Slafer, 2003;Reynolds et al, 2009;Alqudah and Schnurbusch, 2014) because of competition between the spike and stem for limited assimilates (González et al, 2003(González et al, , 2011Ghiglione et al, 2008). Quantitative trait loci with strong effects on the durations of individual preanthesis phases have been mapped close to PHOTOPERIOD1, Ppd-B1/Ppd-D1 and Ppd-H1 in wheat and barley, respectively (González et al, 2005;Borrás-Gelonch et al, 2010Sanna et al, 2014).…”