Photosynthate partitioning to starch in Arabidopsis thaliana is insensitive to light intensity but sensitive to photoperiod due to a restriction on growth in the light in short photoperiods

Abstract

Photoperiod duration can be predicted from previous days, but irradiance fluctuates in an unpredictable manner. To investigate how allocation to starch responds to changes in these two environmental variables, Arabidopsis Col-0 was grown in a 6 h and a 12 h photoperiod at three different irradiances. The absolute rate of starch accumulation increased when photoperiod duration was shortened and when irradiance was increased. The proportion of photosynthate allocated to starch increased strongly when photoperiod duration was decreased but only slightly when irradiance was decreased. There was a small increase in the daytime level of sucrose and twofold increases in glucose, fructose and glucose 6-phosphate at a given irradiance in short photoperiods compared to long photoperiods. The rate of starch accumulation correlated strongly with sucrose and glucose levels in the light, irrespective of whether these sugars were responding to a change in photoperiod or irradiance. Whole plant carbon budget modelling revealed a selective restriction of growth in the light period in short photoperiods. It is proposed that photoperiod sensing, possibly related to the duration of the night, restricts growth in the light period in short photoperiods, increasing allocation to starch and providing more carbon reserves to support metabolism and growth in the long night.

Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves

“…Plants accumulate starch more quickly in short than in long photoperiods to provide a larger C reserve to support maintenance and growth in the long night (Mengin et al, ; Smith & Stitt, ; Sulpice et al, ). It has been proposed that the higher rate of starch accumulation is due to a restriction of growth in the light period in response to short photoperiods or low C availability in the preceding night (Mengin et al, ; Mugford et al, ; Sulpice et al, ). There was previously no evidence that the circadian clock regulates the rate of starch accumulation (Mugford et al, ).…”

“…One possible explanation for the slow starch accumulation in prr7 prr9 and elf3 would be that these mutants do not exhaust their starch during the night and that this results in slower starch accumulation in the light period. However, the slower rate of starch accumulation in wild‐type plants when they are grown in long photoperiods or under high irradiance is accompanied by lower levels of reducing sugars (Mengin et al, ; see below for more references), which is opposite to the metabolic phenotype in prr7 prr9 and, especially, elf3 . This indicates that the day genes or ELF3 have a more direct action on starch accumulation.…”

A dichotomy resolved: Plant growth can control the rate of starch accumulation

“…Other dichotomies include the question “is (a) growth limited by photosynthesis or is (b) photosynthesis limited by growth?” In photosynthetic starch metabolism, the dichotomy is whether starch synthesis is (a) an overflow for when sucrose synthesis cannot keep up with the rates of the rest of photosynthesis or (b) a way to store carbon for respiration and possibly growth at night. In this issue, a significant step forward in understanding this last dichotomy is reported, and surprisingly, it involves an effect of plant growth rate on partitioning of carbon to starch (Mengin et al, ).…”

“…Mengin et al () considered two possible explanations (another dichotomy) for the increased partitioning of carbon to starch in short days. One possibility is that (a) the reduced total carbon fixed during a day would lead to signals that would change partitioning.…”

“…Mengin et al () measured many metabolites and showed a good correlation between several sugars, especially sucrose, and growth rate (but trehalose 6‐phosphate, often identified as signaling sugar status, was not reported). Growth was calculated using a whole‐plant carbon balance model (Sulpice et al, ).…”