A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice

Wataru Yamori; Amane Makino; Toshiharu Shikanai

doi:10.1038/srep20147

journal article Open Access Feb 02, 2016

A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice

Wataru Yamori

Amane Makino Toshiharu Shikanai

Scientific Reports Vol. 6 No. 1 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/srep20147

Abstract

AbstractPlants experience a highly variable light environment over the course of the day. To reveal the molecular mechanisms of their photosynthetic response to fluctuating light, we examined the role of two cyclic electron flows around photosystem I (CEF-PSI)—one depending on PROTON GRADIENT REGULATION 5 (PGR5) and one on NADH dehydrogenase-like complex (NDH)—in photosynthetic regulation under fluctuating light in rice (Oryza sativaL.). The impairment of PGR5-dependent CEF-PSI suppressed the photosynthetic response immediately after sudden irradiation, whereas the impairment of NDH-dependent CEF-PSI did not. However, the impairment of either PGR5-dependent or NDH-dependent CEF-PSl reduced the photosynthetic rate under fluctuating light, leading to photoinhibition at PSI and consequently a reduction in plant biomass. The results highlight that (1) PGR5-dependent CEF-PSI is a key regulator of rapid photosynthetic responses to high light intensity under fluctuating light conditions after constant high light; and (2) both PGR5-dependent and NDH-dependent CEF-PSI have physiological roles in sustaining photosynthesis and plant growth in rice under repeated light fluctuations. The highly responsive regulatory system managed by CEF-PSI appears able to optimize photosynthesis and plant growth under naturally fluctuating light conditions.

Topics

No keywords indexed for this article. Browse by subject →

References

31

[1]

Pearcy, R. W. Sunflecks and photosynthesis in plant canopies. Ann. Rev. Plant Physiol. Plant Mol. Biol. 41, 421–453 (1990). 10.1146/annurev.pp.41.060190.002225

[2]

Shikanai, T. Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant. Biol. 58, 199–217 (2007). 10.1146/annurev.arplant.58.091406.110525

[3]

Munekage, Y. et al. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110, 361–371 (2002). 10.1016/s0092-8674(02)00867-x

[4]

Hertle A. P. et al. PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell 49, 511–523 (2013). 10.1016/j.molcel.2012.11.030

[5]

Shikanai, T. et al. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc. Natl Acad. Sci. USA 95, 9705–9709 (1998). 10.1073/pnas.95.16.9705

[6]

Peng, L., Fukao, Y., Fujiwara, M. & Shikanai, T. Multistep assembly of chloroplast NADH dehydrogenase-like subcomplex A requires several nucleus-encoded proteins, including CRR41 and CRR42, in Arabidopsis. Plant Cell 24, 202–214 (2012). 10.1105/tpc.111.090597

[7]

Munekage, Y. N., Genty, B. & Peltier, G. Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol. 49, 1688–1698 (2008). 10.1093/pcp/pcn140

[8]

Tikkanen, M., Grieco, M., Kangasjärvi, S. & Aro, E. M. Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 152, 723–735 (2010). 10.1104/pp.109.150250

[9]

PROTON GRADIENT REGULATION5 Is Essential for Proper Acclimation of Arabidopsis Photosystem I to Naturally and Artificially Fluctuating Light Conditions

Marjaana Suorsa, Sari Järvi, Michele Grieco et al.

The Plant Cell 2012 10.1105/tpc.112.097162

[10]

Kono, M., Noguchi, K. & Terashima, I. Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol. 55, 990–1004 (2014). 10.1093/pcp/pcu033

[11]

Nishikawa, Y. et al. PGR5-dependent cyclic electron transport around PSI contributes to the redox homeostasis in chloroplasts rather than CO2 fixation and biomass production in rice. Plant Cell Physiol. 53, 2117–2126 (2012). 10.1093/pcp/pcs153

[12]

Munekage, Y. et al. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429, 579–582 (2004). 10.1038/nature02598

[13]

Endo, T., Shikanai, T., Takabayashi, A., Asada, K. & Sato, F. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Letters 457, 5–8 (1999). 10.1016/s0014-5793(99)00989-8

[14]

Wang, P. et al. Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol. 141, 465–474 (2006). 10.1104/pp.105.070490

[15]

Yamori, W., Sakata, N., Suzuki, Y., Shikanai, T. & Makino, A. Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J 68, 966–976 (2011). 10.1111/j.1365-313x.2011.04747.x

[16]

Joliot, P. & Joliot, A. Quantification of cyclic and linear flows in plants. Proc. Natl Acad. Sci. USA 102, 4913–4918 (2005). 10.1073/pnas.0501268102

[17]

Okegawa, Y., Kagawa, Y., Kobayashi, Y. & Shikanai, T. Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol. 49, 825–834 (2008). 10.1093/pcp/pcn055

[18]

Smith, H. Light Quality, Photoperception and Plant Strategy. Annu. Rev. Plant. Physiol. 33, 481–518 (1982). 10.1146/annurev.pp.33.060182.002405

[19]

Terashima, I., Araya, T., Miyazawa, S.-I., Sone, K. & Yano, S. Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Ann. Bot. 95, 507–19 (2005). 10.1093/aob/mci049

[20]

Yamori, W., Evans, J. R. & von Caemmerer, S. Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation rate in tobacco leaves. Plant, Cell & Environ. 33, 332–343 (2010). 10.1111/j.1365-3040.2009.02067.x

[21]

Yamori, W., Masumoto, C., Fukayama, H. & Makino, A. Rubisco activase is a key regulator of non-steady-state photosynthesis at any leaf temperature and, to a lesser extent, of steady-state photosynthesis at high temperature. Plant J. 71, 870–880 (2012). 10.1111/j.1365-313x.2012.05041.x

[22]

Buchanan, B. B. & Balmer, Y. Redox regulation: a broadening horizon. Annu. Rev. Plant. Biol. 56, 187–220 (2005). 10.1146/annurev.arplant.56.032604.144246

[23]

Hubbart, S., Ajigboye, O. O., Horton, P. & Murchie, E. H. The photoprotective protein PsbS exerts control over CO2 assimilation rate in fluctuating light in rice. Plant J. 71, 402–412 (2012). 10.1111/j.1365-313x.2012.04995.x

[24]

Makino, A., Miyake, C. & Yokota, A. Physiological functions of the water-water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant Cell Physiol. 43, 1017–1026 (2002). 10.1093/pcp/pcf124

[25]

Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light

Wataru Yamori, Toshiharu Shikanai, Amane Makino

Scientific Reports 2015 10.1038/srep13908

[26]

Shikanai, T. Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr. Opin. Biotech. 26, 25–30 (2014). 10.1016/j.copbio.2013.08.012

[27]

Tikkanen, M. & Aro, E. M. Integrative regulatory network of plant thylakoid energy transduction. Trends Plant Sci. 19, 10–17 (2014). 10.1016/j.tplants.2013.09.003

[28]

Allahverdiyeva, Y., Suorsa, M., Tikkanen, M. & Aro, E.-M. Photoprotection of photosystems in fluctuating light intensities. J. Exp. Bot. 66, 2427–2436 (2015). 10.1093/jxb/eru463

[29]

Yamori, W. & Shikanai, T. Physiological Functions of Cyclic Electron Transport Around Photosystem I in Sustaining Photosynthesis and Plant Growth. Annu. Rev. Plant. Biol. 67 (2016) (in press). 10.1146/annurev-arplant-043015-112002

[30]

Wang, C., Yamamoto, H. & Shikanai, T. Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim. Biophys. Acta 1847, 931–938 (2015). 10.1016/j.bbabio.2014.11.013

[31]

Klughammer, C. & Schreiber, U. Analysis of light induced absorbance changes in the near-infrared region. I. Characterization of various components in isolated chloroplasts. Z Naturforsch 46c, 233–244 (1991). 10.1515/znc-1991-3-413

Cited By

255

Distinct contribution of two cyclic electron transport pathways to P700 oxidation

Qi Zhou, Hiroshi Yamamoto · 2022

Plant Physiology

Efficient photosynthesis in dynamic light environments: a chloroplast's perspective

Elias Kaiser, Viviana Correa Galvis · 2019

Biochemical Journal

Contribution of Cyclic and Pseudo-cyclic Electron Transport to the Formation of Proton Motive Force in Chloroplasts

Toshiharu Shikanai, Hiroshi Yamamoto · 2017

Molecular Plant

The Role of Na+ and K+ Transporters in Salt Stress Adaptation in Glycophytes

Dekoum V. M. Assaha, Akihiro Ueda · 2017

Frontiers in Physiology

Metrics

255

Citations

31

References

Details

Published: Feb 02, 2016
Vol/Issue: 6(1)
License: View

Authors

Department of Botany, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan

Cite This Article

Wataru Yamori, Amane Makino, Toshiharu Shikanai (2016). A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Scientific Reports, 6(1). https://doi.org/10.1038/srep20147

A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice

You May Also Like