Editorial overview: Physiology and metabolism: Light responses from photoreceptors to photosynthesis and photoprotection

Editorial overview: Physiology and metabolism: Light responses from photoreceptors to photosynthesis and photoprotection

COPLBI-1594; NO. OF PAGES 3 Available online at www.sciencedirect.com ScienceDirect Editorial overview: Physiology and metabolism: Light responses f...

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COPLBI-1594; NO. OF PAGES 3

Available online at www.sciencedirect.com

ScienceDirect Editorial overview: Physiology and metabolism: Light responses from photoreceptors to photosynthesis and photoprotection Krishna K Niyogi Current Opinion in Plant Biology 2017, 37:xx–yy

http://dx.doi.org/10.1016/j.pbi.2017.05.009 1369-5266/ã 2017 Elsevier Ltd. All rights reserved.

Krishna K Niyogi1,2 1

Howard Hughes Medical Institute, Department of Plant and Microbial Biology, University of California Berkeley, Berkeley, CA 94720-3102, USA 2

Molecular Biophysics and Integrated Bioimaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA e-mail: [email protected]

Kris Niyogi is an HHMI investigator, professor and chair of the Department of Plant and Microbial Biology at UC-Berkeley, and a faculty scientist at Lawrence Berkeley National Laboratory. His research focuses on understanding the regulation of photosynthesis and photoprotection with the goal of improving photosynthetic efficiency and crop productivity.

The conversion of sunlight, carbon dioxide, and water into chemical energy and biomass in oxygenic photosynthesis is the defining metabolism of plants, algae, and cyanobacteria. Oxygenic photosynthesis was invented by prokaryotic cyanobacteria, and it moved into eukaryotes via endosymbiosis, beginning about a billion years ago [1]. The engulfed cyanobacterium evolved into the organelle known as the chloroplast in Archaeplastida, which includes green algae and plants, and subsequent secondary (and even tertiary) endosymbiosis events spread chloroplasts and photosynthesis to other eukaryotic supergroups in the tree of life [2]. Along with the evolution and radiation of oxygenic photosynthesis, these photosynthetic organisms elaborated diverse mechanisms to perceive and respond to light in various ways to increase light capture for photosynthesis or to protect against oxidative damage caused by excess light. This issue focuses on the mechanisms that oxygenic photosynthetic organisms use to perceive and respond to the spectrum and intensity of incident light in order to regulate photosynthesis and photoprotection. Investigation of these light responses is critical for understanding the basic physiology and metabolism of plants, algae, and cyanobacteria, and it provides a foundation for rational engineering of photosynthesis and photoprotection to improve crop productivity. In many instances, responses to light are mediated by specific photoreceptors, such as phytochromes, cryptochromes, phototropins, aureochromes, rhodopsin-like photoreceptors, and the UV-B photoreceptor UVR8. Phytochromes are arguably the best known photoreceptors in plants, and Rockwell and Lagarias [3] describe recent structural insights into phytochrome signaling and discuss the complex and fascinating evolutionary history of phytochromes in cyanobacteria and eukaryotic algae. Although one might expect that eukaryotic algal and plant phytochromes evolved from a cyanobacterial phytochrome acquired during endosymbiosis, it appears that they might instead be derived from an ancient eukaryotic host phytochrome. Jaubert et al. [4] review the vast diversity of photoreceptors found in marine algae and the roles they play in adaptation to the marine environment. Photoperiod sensing is one important output of light information perceived by photoreceptors, and the evolution of this function and its contribution to circadian clocks in algae and plants are covered by Serrano-Bueno et al. [5]. Focusing on plants, Hoecker [6] describes how the E3 ubiquitin ligase COP1/SPA represses light signaling by marking specific transcription factors (e.g. HY5) for degradation. The COP1/SPA

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2 Physiology and metabolism

complex functions downstream of phytochrome and cryptochrome photoreceptors as a central regulator of photomorphogenesis. Movements in response to light are among the most obvious responses of photosynthetic organisms. These movements include phototaxis and phototropism, as well as chloroplast movements, that can optimize light capture for photosynthesis, or minimize light absorption as a photoprotective mechanism. A particularly dramatic example of light-induced movement in plants is solar tracking (heliotropism) in sunflower, which increases photosynthetic productivity [7], but even cyanobacteria can move in response to light. Schuergers et al. [8] describe the mechanism and regulation of phototaxis in cyanobacteria, which lack flagella. In addition to exhibiting phototaxis, some cyanobacteria have the ability to tune the pigment composition of their photosynthetic light-harvesting antenna and/or photosystems to match the spectrum of light that is available. The article by Montgomery [9] reviews recent progress in understanding chromatic acclimation, a photomorphogenesis process in which cyanobacteria adjust the composition of their light-harvesting phycobilisomes in response to the wavelength of available light. There are now five recognized types of chromatic acclimation that respond to light ranging from blue to far-red. Ho et al. [10] describe the astonishing number and diversity of cyanobacterial photoreceptors that regulate chromatic acclimation, and they focus on a newly discovered type called far-red light photoacclimation (FaRLiP). Cyanobacteria that are capable of performing FaRLiP synthesize unusual far-red-absorbing pigments using enzymes and regulators that are encoded in a gene cluster. Pigment biosynthesis in plants is also regulated by light. As described by Llorente et al. [11], the synthesis and accumulation of carotenoids is controlled by the transcription factors PIF1, HY5, and PAR1, which regulate expression of the PSY gene encoding phytoene synthase, the committed enzymatic step in carotenoid biosynthesis. Interestingly, the control by PIF1 appears to be important not only in leaves, but also during fruit ripening. Light is necessary for photosynthesis, and light harvesting in eukaryotic algae and plants is mainly accomplished by members of the light-harvesting complex (LHC) protein superfamily [12]. Iwai and Yokono [13] describe the diverse complement of LHC proteins in the moss Physcomitrella patens, which occupies, as an early land plant, an interesting evolutionary position between eukaryotic algae and vascular land plants. Comparison of LHC proteins in P. patens with those in the green alga Chlamydomonas reinhardtii and the model plant Arabidopsis thaliana provides insights into features of photosynthetic light harvesting, electron transport, and photoprotection Current Opinion in Plant Biology 2017, 37:1–3

that might have been important during the transition from an aquatic environment to land. In nature, oxygenic photosynthesis is much more complicated than the straightforward Z-scheme presented in most textbooks, and there are several alternative electron transport pathways that contribute to the regulation and photoprotection of photosynthesis. These pathways include cyclic electron transport and routes that deliver electrons to oxygen as an acceptor. Several of these pathways serve as safety valves or sinks for excess electrons [14]. Alric and Johnson [15] review the current state of our understanding of these alternative pathways, which have important functions in fluctuating light and excess light, and Armbruster et al. [16] focus on how these different electron transport pathways and recently identified transporters in photosynthetic membranes affect the generation and maintenance of a proton motive force, which not only drives ATP synthesis in chloroplasts but also regulates photoprotection when light absorption exceeds photosynthetic capacity. Photosynthetic capacity is generally upregulated in plants that are grown in high light vs. limiting light. DemmigAdams et al. [17] describe how this upregulation involves concomitant increases in the capacity for vascular transport of photosynthetic products and sink strength in the context of whole-plant physiology. Although cyanobacteria, eukaryotic algae, and plants need light for photosynthesis, light in excess of their photosynthetic capacity can cause photoinhibition. Therefore, these organisms have evolved photoprotective mechanisms that safely dissipate excess excitation energy and electrons. Bao et al. [18] describe the remarkable progress that has been made in understanding how cyanobacteria use the orange carotenoid protein (OCP) for thermal dissipation of excess light absorbed by phycobilisomes. Intriguingly, OCP is a modular protein with two structural domains that are found in different proteins in diverse cyanobacteria. In eukaryotic algae and plants, specific LHC family members such as PSBS and LHCSR function in photoprotection [19]. Allorent and Petroutsos [20] summarize recent studies showing that induction of PSBS and LHCSR expression by excess light in C. reinhardtii is regulated by photoreceptors, namely phototropin and UVR8. These exciting findings establish a functional link between light perception by photoreceptors and expression of proteins needed for photoprotection. Yin and Ulm [21] focus on the role of the UVR8 photoreceptor in sensing and responding to UV-B light, a pathway that involves COP1 and is conserved in C. reinhardtii and plants. Light signaling has been a topic of interest to plant biologists for a very long time, but there has been a recent proliferation of new insights into the diversity of photoreceptors that perceive light in oxygenic photosynthetic www.sciencedirect.com

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Editorial overview Niyogi 3

organisms and their downstream targets that regulate physiology and metabolism. I hope the excitement of these discoveries is reflected in this issue.

11. Llorente B, Martinez-Garcia JF, Stange C, RodriguezConcepcion M: Illuminating colors: regulation of carotenoid biosynthesis and accumulation by light. Curr. Opin. Plant Biol. 2017, 37:49-55.

References

12. Neilson JAD, Durnford DG: Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes. Photosynth. Res. 2010, 106:57-71.

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Shih PM, Matzke NJ: Primary endosymbiosis events date to the later Proterozoic with cross-calibrated phylogenetic dating of duplicated ATPase proteins. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:12355-12360.

13. Iwai M, Yokono M: Light-harvesting antenna complexes in the moss Physcomitrella patens: implications for the evolutionary transition from green algae to land plants. Curr. Opin. Plant Biol. 2017, 37:94-101.

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Keeling PJ: The number, speed, and impact of plastid endosymbioses in eukaryotic evolution. Annu. Rev. Plant Biol. 2013, 64:583-607.

14. Niyogi KK: Safety valves for photosynthesis. Curr. Opin. Plant Biol. 2000, 3:455-460.

3.

Rockwell NC, Lagarias JC: Phytochrome diversification in cyanobacteria and eukaryotic algae. Curr. Opin. Plant Biol. 2017, 37:87-93.

4.

Jaubert M, Bouly J-P, Ribera d’Alcala` M, Falciatore A: Light sensing and responses in marine microalgae. Curr. Opin. Plant Biol. 2017, 37:70-77.

16. Armbruster U, Correa Galvis V, Kunz H-H, Strand DD: The regulation of the chloroplast proton motive force plays a key role for photosynthesis in fluctuating light. Curr. Opin. Plant Biol. 2017, 37:56-62.

5.

Serrano-Bueno G, Romero-Campero FJ, Lucas-Reina E, Romero JM, Valverde F: Evolution of photoperiod sensing in plants and algae. Curr. Opin. Plant Biol. 2017, 37:10-17.

17. Demmig-Adams B, Stewart JJ, Adams WW III: Environmental regulation of intrinsic photosynthetic capacity: an integrated view. Curr. Opin. Plant Biol. 2017, 37:34-41.

6.

Hoecker U: The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr. Opin. Plant Biol. 2017, 37:63-69.

18. Bao H, Melnicki MR, Kerfeld CA: Structure and functions of orange carotenoid protein homologs in cyanobacteria. Curr. Opin. Plant Biol. 2017, 37:1-9.

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Atamian HS, Creux NM, Brown EA, Garner AG, Blackman BK, Harmer SL: Circadian regulation of sunflower heliotropism, floral orientation, and pollinator visits. Science 2016, 353: 587-590.

19. Niyogi KK, Truong TB: Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr. Opin. Plant Biol. 2013, 16: 307-314.

8.

Schuergers N, Mullineaux CW, Wilde A: Cyanobacteria in motion. Curr. Opin. Plant Biol. 2017, 37:109-115.

20. Allorent G, Petroutsos D: Photoreceptor-dependent regulation of photoprotection. Curr. Opin. Plant Biol. 2017, 37:102-108.

9.

Montgomery BL: Seeing new light: recent insights into the occurrence and regulation of chromatic acclimation in cyanobacteria. Curr. Opin. Plant Biol. 2017, 37:18-23.

21. Yin R, Ulm R: How plants cope with UV-B: from perception to response. Curr. Opin. Plant Biol. 2017, 37:42-48.

15. Alric J, Johnson X: Alternative electron transport pathways in photosynthesis: a confluence of regulation. Curr. Opin. Plant Biol. 2017, 37:78-86.

10. Ho M-Y, Soulier NT, Canniffe DP, Shen G, Bryant DA: Light regulation of pigment and photosystem biosynthesis in cyanobacteria. Curr. Opin. Plant Biol. 2017, 37:24-33.

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Please cite this article in press as: Niyogi KK: Editorial overview: Physiology and metabolism: Light responses from photoreceptors to photosynthesis and photoprotection, Curr Opin Plant Biol (2017), http://dx.doi.org/10.1016/j.pbi.2017.05.009