Understanding phytochrome regulation of plant growth and carbon resource management in Arabidopsis Thaliana

Abstract

Plantshave the ability to monitor fluctuations in their light environment constantlyand actively adjust their metabolism to cope with variations in light andcarbon (C) resource availability. Phytochromes (phys), red and far-redphotoreceptors, are known to regulate major physiological and plastic growthresponses through the plant life cycle. It is well established that phytochromecontrol shade avoidance response (SAR), characterised by petiole elongation,reduction in leaf blade, and hyponasty. These large-scale changes in plantarchitecture are accompanied by parallel adjustments in C-resources. Despiteobvious interconnectedness, the link between phytochrome signaling pathways andcentral metabolism remains largely unknown. Previous work in our lab has shownthat phy deficiency results in a dramatic reduction in biomass and an alteredC-metabolism due to over-accumulation of end of the day (EOD) sucrose andstarch in adult plants.

Inthis thesis, I use single and multiple phytochrome loss of function mutants toexplore how phytochromes interact with C metabolism to control plant growth anddevelopment. Consistent with the previous work from our lab, I show thatphytochrome depletion has a profound impact on plant growth and biomass. Myanalysis further revealed that phyB isthe key determinant biomass and leaf production rate. Despite dramaticallyreduced biomass, particularly in multiple phymutants, accumulation of sucrose and starch led us to reason that phenotypicand metabolic changes in adult phymutants could arise due to 1) an inability to utilise their C-resources thatmay result in growth impairment and reduced biomass, or 2) slow growth of phy mutants coupled with low demand forresources leads to over-accumulation of sucrose/starch. Ourprotein data of adult phytochrome mutants established that phy mutants appear to accumulate normal levels of protein,suggesting that resources are accessible in phydeficient plants and that growth is unlikely to be affected in adult phy mutants. However, the lower proteincontent of young phy mutants andadult mutants grown under the low light conditions that show a constrainedgrowth suggests that a resource limitation has a lasting impact on biomassproduction.

Analysisof publicly available microarray (phyBmutant seedlings) and RNA-seq (phyABCDEmutant seedlings) data illustrate that phyBand higher-order phyABCDE mutantshave significantly altered expression (50% and 60%,respectively) of the global carbon starvation transcriptome. Using nightextension starvation conditions and end-of-day far-red treatments (EoD-FR), Iverified this experimentally and further shown that even though phy mutant seedlings have fewerresources, phytochrome regulation of starvation genes is independent ofinternal carbon status. Follow on analysis indicates that phytochrome signalingmay control starvation genes, at least partly through bZIP1 – a component ofthe SnRK1 pathway, and this response appears to potentially involved clockcomponents, CCA1 and LHY. In summary, this study uncovers the molecularcomponents that link phytochrome with plant carbon sensing network, providing anovel route for phytochrome to adjust metabolism and potentially modify growthaccording to the prevailing light environment. These findings bring a newperspective into phytochrome research, suggesting the potential application ofsuch knowledge to crop improvement in the future.