Phytochrome Control of Resource Allocation and Growth in Arabidopsis and in Brassicaceae crops
Final Report Abstract
For plants, light is a signal that carries information about the environment, and a source of energy for photosynthesis. The PHYTOCAL project explored how light signalling and photosynthesis are coordinated to achieve carbon resource management and growth over the varied light conditions that plant experience everyday. PHYTOCAL researchers have shown that the phytochrome light receptors control carbon resource allocation to leaves, and metabolic flux to stress metabolites, sugars and starch, a major carbon reserve in plants. Light irradiance levels, and particularly photoperiod length governs the proportion of carbon that is stored as starch. The photoperiodic mechanism, which comprises light receptor and circadian clock interactions, ensures sufficient starch is synthesised during short photoperiods to prevent starvation during long (winter) nights. In natural dawns, where light intensity rises gradually, clock rephrasing prevents carbon starvation around dawn, before photosynthesis is initiated. We have shown phytochrome is a potent modulator of the genome-wide carbon starvation response. Here phytochrome operates in concert with the clock to antagonise starvation-mediated gene expression. ELF3 (EARLY FLOWERING 3), the circadian clock evening complex component, is known to transcriptionally regulate light controlled PIF (PHYTOCHROME INTERACTING FACTOR) genes. We have learned that that ELF3 and PIFs, are regulated by the plants internal carbon status, they control the morning phase-rise in reducing sugars, the allocation to starch. The ELF3-PIF module therefore fulfils an important role in coupling carbon resource availability to growth. The project has validated B. rapa as a crop model with a conserved phytochrome-carbon network. This work showed that elevated CO2 has a dramatic impact on B. rapa growth and resource allocation, and that BrphyB is a centrally positioned regulator of these CO2-elicited responses. We exploited the upright stature of B. rapa to document the dynamic transcriptome-level changes that occur in canopy leaves that have been occluded from light. Our data showed that occlusion strongly induced genes involved in autophagy, catabolism and leaf senescence, and supressed genes involved in photosynthesis, metabolism and translation. These findings indicate that leaf masking, which occurs frequently in nature, drives a shift from carbon fixation and nutrient acquisition toward redistribution of cellular resources. We established that BrphyB signalling contributes to this reprogramming by regulating processes including translation, peptide and cellular biosynthesis. Further, BrphyB action is important for photosynthetic machinery recovery when covered leaves are re-exposed to light. PrphyB therefore contributes to dynamic carbon-resource allocation during and after canopy leaf shading. Model-based analysis has generated new conceptual insights into how the light and clock pathways control metabolism and growth. For instance, we established that the sizeable impact of phytochrome action on final plant biomass is determined solely at the seedling stage. This work points to the critical role of phytochrome during seedling establishment, and setting the initial pace of biomass accumulation. We have generated a new photoperiodic model that links PHYA to the circadian clock through the carbon responsive ELF3-PIF module. This phyA-based “external coincidence” model provides sensitive detection of photoperiod length, and the induction of (secondary metabolite) flavonoid pathway gene expression, specifically in short days.
Publications
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Photoreceptor effects on plant biomass, resource allocation, and metabolic state. Proc Natl Acad Sci USA. 2016 Jul 5;113(27):7667-72
Yang D, Seaton DD, Krahmer J, Halliday KJ
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(2017) .Getting back to nature: a reality check for experiments in controlled environments. J, Exp. Bot 68, 4463-4477
Annunziata, M.G., Apelt, F., Carillo, P., Mengin, V., Kraus, U., Feil, R., Mengin, V., Lauxmann, M-A., Köhl, K., Nikoloski, Z., Stitt, M., and Lunn, J.E.
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(2017) Photosynthate Partitioning to Starch in Arabidopsis is Insensitive to Light Intensity but Sensitive to Photoperiod due to a Restriction on Growth in the Light in Short Photoperiods. Plant Cell Environ.
Mengin, V., Pyl. E.-T., Moraes, T.-A., Sulpice, R., Krohn, N., Encke, B and Stitt, M
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(2018) Response of Arabidopsis primary metabolism and the clock to low night temperature in a natural light environment. J. Exp. Bot. 20, 4881-4895
Annunziata, M.G., Apelt, F., Carillo, P., Krause ,U., Feil , R., Koehl, K., Lunn, J.E. and Stitt M.
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Dawn and photoperiod sensing by phytochrome A. Proc Natl Acad Sci USA. 2018 Oct 9;115(41):10523-10528
Seaton DD, Toledo-Ortiz G, Ganpudi A, Kubota A, Imaizumi T, Halliday KJ
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Phytochrome B regulates resource allocation in Brassica rapa. J Exp Bot. 2018 May 19;69(11):2837-2846
Arsovski AA, Zemke JE, Haagen BD, Kim SH, Nemhauser JL
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Phytochrome, Carbon Sensing, Metabolism, and Plant Growth Plasticity. Plant Physiol. 2018 Feb;176(2):1039-1048
Krahmer J, Ganpudi A, Abbas A, Romanowski A, Halliday KJ
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(2019) Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves. Plant Cell Environ. 42, 549-573
Flis, A, Mengin, V., Ivakov, A.A., Mugford, S, Hubberten, H-M., Encke, B., Krohn, K., Höhne, M., Feil, R., Hoefgen, R., Lunn, J.E., Millar, A.J., Smith, A.M., Sulpice, R. and Stitt, M.
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(2019) Response of the circadian clock and diel starch turnover to a day of low light or CO2 in Arabidopsis. Plant Physiol. 179, 1457–1478
Moraes, T, A., Mengin, V., Annunziate, M.G., Encke, B., Krohn, N., Höhne, M. and Stitt, M.
