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      Photoreceptor effects on plant biomass, resource allocation, and metabolic state

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          Significance

          Plant development is inextricably bound to the external light environment. Light drives photosynthetic carbon fixation and activates a suite of signal-transducing photoreceptors that regulate plant growth and development. This study highlights an important role for the phytochrome light receptors in synchronizing carbon resource allocation to daytime growth. We establish that phytochromes are major environmental drivers of plant biomass production and regulate the transition between growth-intensive and stress-resilient states.

          Abstract

          Plants sense the light environment through an ensemble of photoreceptors. Members of the phytochrome class of light receptors are known to play a critical role in seedling establishment, and are among the best-characterized plant signaling components. Phytochromes also regulate adult plant growth; however, our knowledge of this process is rather fragmented. This study demonstrates that phytochrome controls carbon allocation and biomass production in the developing plant. Phytochrome mutants have a reduced CO 2 uptake, yet overaccumulate daytime sucrose and starch. This finding suggests that even though carbon fixation is impeded, the available carbon resources are not fully used for growth during the day. Supporting this notion, phytochrome depletion alters the proportion of day:night growth. In addition, phytochrome loss leads to sizeable reductions in overall growth, dry weight, total protein levels, and the expression of CELLULOSE SYNTHASE-LIKE genes. Because cellulose and protein are major constituents of plant biomass, our data point to an important role for phytochrome in regulating these fundamental components of plant productivity. We show that phytochrome loss impacts core metabolism, leading to elevated levels of tricarboxylic acid cycle intermediates, amino acids, sugar derivatives, and notably the stress metabolites proline and raffinose. Furthermore, the already growth-retarded phytochrome mutants are less responsive to growth-inhibiting abiotic stresses and have elevated expression of stress marker genes. This coordinated response appears to divert resources from energetically costly biomass production to improve resilience. In nature, this strategy may be activated in phytochrome-disabling, vegetation-dense habitats to enhance survival in potentially resource-limiting conditions.

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          Author and article information

          Journal
          Proc Natl Acad Sci U S A
          Proc. Natl. Acad. Sci. U.S.A
          pnas
          pnas
          PNAS
          Proceedings of the National Academy of Sciences of the United States of America
          National Academy of Sciences
          0027-8424
          1091-6490
          5 July 2016
          21 June 2016
          : 113
          : 27
          : 7667-7672
          Affiliations
          [1] aSynthSys, School of Biological Sciences, University of Edinburgh , Edinburgh EH9 3BF, United Kingdom
          Author notes
          1To whom correspondence should be addressed. Email: karen.halliday@ 123456ed.ac.uk .

          Edited by Winslow R. Briggs, Carnegie Institution for Science, Stanford, CA, and approved May 17, 2016 (received for review January 30, 2016)

          Author contributions: D.Y. and K.J.H. designed research; D.Y. and J.K. performed research; D.Y., D.D.S., and K.J.H. analyzed data; and D.Y. and K.J.H. wrote the paper.

          Article
          PMC4941476 PMC4941476 4941476 201601309
          10.1073/pnas.1601309113
          4941476
          27330114
          146b0f1b-a78f-476f-92f7-316d517dbe4a
          Page count
          Pages: 6
          Funding
          Funded by: Biotechnology and Biological Sciences Research Council (BBSRC) 501100000268
          Award ID: BB/F005237/1
          Categories
          Biological Sciences
          Plant Biology
          From the Cover

          sucrose, growth, phytochrome, light, Arabidopsis thaliana

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