phot1 and phot2 mediate blue light regulation of stomatal opening
Abstract
The stomatal pores of higher plants allow for gaseous exchange into and out of leaves. Situated in the epidermis, they are surrounded by a pair of guard cells which control their opening in response to many environmental stimuli, including blue light. Opening of the pores is mediated by K(+) accumulation in guard cells through a K(+) channel and driven by an inside-negative electrical potential. Blue light causes phosphorylation and activation of the plasma membrane H(+)-ATPase that creates this potential. Thus far, no blue light receptor mediating stomatal opening has been identified, although the carotenoid, zeaxanthin, has been proposed. Arabidopsis mutants deficient in specific blue-light-mediated responses have identified four blue light receptors, cryptochrome 1 (cry1), cryptochrome 2 (cry2), phot1 and phot2. Here we show that in a double mutant of phot1 and phot2 stomata do not respond to blue light although single mutants are phenotypically normal. These results demonstrate that phot1 and phot2 act redundantly as blue light receptors mediating stomatal opening.
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Stomatal opening is regulated by the functional redundancy of PHOT1 and PHOT2.
“Stomatal opening is regulated by the functional redundancy of PHOT1 and PHOT2”
From The action of enhancing weak light capture via phototropic growth and chloroplast movement in plants (2022) · cites this paper as Kinoshita et al., 2001
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BackgroundA Mechanism for Reorientation of Cortical Microtubule Arrays Driven by Microtubule Severing
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“Unlike cry1cry2, the phot1phot2 mutant is blocked in the phototropin-dependent chloroplast, stomatal, and phototropic movements and lacks blue-light induction of calcium currents in mesophyll cells (Kinoshita et al., 2001; Sakai et al., 2001; Stoelzle et al., 2003).”
BackgroundFedorov, R., Schlichting, I., Hartmann, E., Domratcheva, T. M., Fuhrmann, M., & Hegemann, P. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)75052-8 · Cited by 267 · see citing works
“…membraneassociated proteins that function as primary photoreceptor for phototropic plant movement (Huala et al., 1997; Christie et al., 1998; Christie et al., 1999), chloroplast relocation (Jarillo et al., 2001; Kagawa et al., 2001), and stomatal opening in guard cells (Kinoshita et al., 2001).”
BackgroundLight perception in plant disease defence signalling
Karpiński, S. M., Gabryś, H., Mateo, A., Karpińska, B., & Mullineaux, P. M. (2003) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(03)00061-x · Cited by 264 · see citing works
From seed to seed: the role of photoreceptors in Arabidopsis development
Sullivan, J. A., & Deng, X. W. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00212-4 · Cited by 264 · see citing works
“While phot1 and phot2 single mutants show only small changes in blue light-induced stomatal opening, this response is completely absent in a phot1phot2 double mutant (Kinoshita et al., 2001).”
BackgroundAUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles
Takahashi, F., Yamagata, D., Ishikawa, M., Fukamatsu, Y., Ogura, Y., Kasahara, M., Kiyosue, T., Kikuyama, M., Wada, M., & Kataoka, H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707692104 · Cited by 263 · see citing works
Self-citationKiba, T., Henriques, R., Sakakibara, H., & Chua, N. (2007) · The Plant Cell · doi:10.1105/tpc.107.053033 · Cited by 261 · see citing works
“, 1999), phot1 phot2 (Kinoshita et al., 2001), and phyA phyB (Devlin et al.”
BackgroundInfluentialLi, H., Xu, Z., & Tang, C. (2010) · Plant Cell Tissue and Organ Culture (PCTOC) · doi:10.1007/s11240-010-9763-z · Cited by 261 · see citing works
“In addition, blue light was received directly by phototropins and activated a signaling cascade that resulted in fast stomata opening under background red light (Kinoshita et al. 2001; Doi et al. 2004; Shimazaki et al. 2007).”
BackgroundPennisi, G., Blasioli, S., Cellini, A., Maia, L., Crepaldi, A., Braschi, I., Spinelli, F., Nicola, S., Fernández, J. A., Stanghellini, C., et al. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00305 · Cited by 260 · see citing works
Receptor quality control in the endoplasmic reticulum for plant innate immunity
Saijo, Y., Tintor, N., Lu, X., Rauf, P., Pajerowska-Mukhtar, K. M., Häweker, H., Dong, X., Robatzek, S., & Schulze‐Lefert, P. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.263 · Cited by 259 · see citing works
“Anti-FLS2 and AHA2 antibodies were described elsewhere (Kinoshita et al, 2001; Chinchilla et al, 2006).”
BackgroundEvidence for Involvement of Photosynthetic Processes in the Stomatal Response to CO2
Messinger, S. M., Buckley, T. N., & Mott, K. A. (2006) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.073676 · Cited by 255 · see citing works
“The receptor for this response has yet to be identified unequivocally, and there is evidence supporting both zeaxanthin (Zeiger and Zhu, 1998; Talbott et al., 2003) and phototropins (Kinoshita et al., 2001; Doi et al., 2004) for this role.”
BackgroundContributions of green light to plant growth and development
Wang, Y., & Folta, K. M. (2013) · American Journal of Botany · doi:10.3732/ajb.1200354 · Cited by 249 · see citing works
Modulation of environmental responses of plants by circadian clocks
Hotta, C. T., GARDNER, M. J., Hubbard, K., BAEK, S. J., Dalchau, N., Suhita, D., Dodd, A. N., & Webb, A. A. R. (2007) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2006.01627.x · Cited by 247 · see citing works
“CONSTITUTIVELY PHOTOMORPHOGENIC 1 (COP1) is believed to function in a similar light transduction pathway as DET1.”
BackgroundInfluentialPhot-LOV1: Photocycle of a Blue-Light Receptor Domain from the Green Alga Chlamydomonas reinhardtii
Kottke, T., Heberle, J., Hehn, D., Dick, B., & Hegemann, P. (2003) · Biophysical Journal · doi:10.1016/s0006-3495(03)74933-9 · Cited by 246 · see citing works
“Phototropins and homologs, recently renamed Phot proteins (Briggs et al., 2001), comprise a class of blue-light receptors that are involved in phototropic plant movement (Christie et al., 1998, 1999; Huala et al., 1997), chloroplast relocation (Jarillo et al., 2001; Kagawa et al., 2001), and stomatal opening in guard…”
BackgroundRoles of ion channels and transporters in guard cell signal transduction
Pandey, S., Zhang, W., & Assmann, S. M. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.04.008 · Cited by 245 · see citing works
“light signal upstream of the type 1 protein phosphatase came when studies with the double blue light-receptor mutant phot1 phot2 demonstrated essentially no blue light-stimulated stomatal opening in this mutant [12].”
Spatio‐temporally precise activation of engineered receptor tyrosine kinases by light
Grusch, M., Schelch, K., Riedler, R., Reichhart, E., Differ, C., Berger, W., Inglés‐Prieto, Á., & Janovjak, H. (2014) · The EMBO Journal · doi:10.15252/embj.201387695 · Cited by 245 · see citing works
“…domains such as enzymes [for instance, in the flowering plant Arabidopsis thaliana and the green alga Chlamydomonas reinhardtii (Huang et al, 2002; Kinoshita et al, 2001)] or transcriptional regulators [for instance, in the fungus Neurospora crassa and the yellow-green alga Vaucheria frigida…”
BackgroundBuckley, T. N. (2017) · PLANT PHYSIOLOGY · doi:10.1104/pp.16.01772 · Cited by 245 · see citing works
“…example, CO2 responses persist in darkness (Heath and Russell, 1954; Messinger et al., 2006), and the existence of a distinct low-fluence and photosynthesis-independent response to blue light was established many years ago (Shimazaki et al., 1986; Kinoshita et al., 2001; Inoue and Kinoshita, 2017).”
BackgroundBlue light-induced autophosphorylation of phototropin is a primary step for signaling
Inoue, S.-I., Kinoshita, T., Matsumoto, M., Nakayama, K. I., Doi, M., & Shimazaki, K.-I. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709189105 · Cited by 269 · see citing works
Self-citationThe pH of the Apoplast: Dynamic Factor with Functional Impact Under Stress
Geilfus, C. (2017) · Molecular Plant · doi:10.1016/j.molp.2017.09.018 · Cited by 240 · see citing works
The FOX hunting system: an alternative gain‐of‐function gene hunting technique
Ichikawa, T., Nakazawa, M., Kawashima, M., Iizumi, H., Kuroda, H., Kondou, Y., Tsuhara, Y., Suzuki, K., Ishikawa, A., Seki, M., et al. (2006) · The Plant Journal · doi:10.1111/j.1365-313x.2006.02924.x · Cited by 238 · see citing works
Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leaves
Savvides, A. M., Fanourakis, D., & van Ieperen, W. (2011) · Journal of Experimental Botany · doi:10.1093/jxb/err348 · Cited by 232 · see citing works
Responses of ferns to red light are mediated by an unconventional photoreceptor
Kawai, H., Kanegae, T., Christensen, S., Kiyosue, T., Sato, Y., Imaizumi, T., Kadota, A., & Wada, M. (2003) · Nature · doi:10.1038/nature01310 · Cited by 231 · see citing works
Self-citationWang, Y., Noguchi, K., Ono, N., Inoue, S., Terashima, I., & Kinoshita, T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305438111 · Cited by 228 · see citing works
“To produce transgenic plants showing enhanced stomatal opening in response to light, we attempted to express three key components of stomatal opening: PHOTOTROPIN 2 (PHOT2), an isoform of the blue light receptor phototropin (13); ARABIDOPSIS H-ATPASE 2 (AHA2), a typical isoform of the plasma membrane H-ATPase (24); an…”
BackgroundSelf-citationBlue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening
Horrer, D., Flütsch, S., Pazmiño, D. M., Matthews, J. S. A., Thalmann, M., Nigro, A., Leonhardt, N., Lawson, T., & Santelia, D. (2016) · Current Biology · doi:10.1016/j.cub.2015.12.036 · Cited by 227 · see citing works
“opened to a greater extent in the presence of 10 μM Fc (Figure 4E)[29].”
Phylogenomic Evidence for the Monophyly of Bryophytes and the Reductive Evolution of Stomata
Harris, B. J., Harrison, C. J. O., Hetherington, A. M., & Williams, T. A. (2020) · Current Biology · doi:10.1016/j.cub.2020.03.048 · Cited by 227 · see citing works
Phosphorylation of BLUS1 kinase by phototropins is a primary step in stomatal opening
Takemiya, A., Sugiyama, N., Fujimoto, H., Tsutsumi, T., Yamauchi, S., Hiyama, A., Tada, Y., Christie, J. M., & Shimazaki, K.-I. (2013) · Nature Communications · doi:10.1038/ncomms3094 · Cited by 219 · see citing works
“B1N; N-terminal fragment of BLUS1 (amino acids 1-294), B1C; C-terminal fragment of BLUS1 (294-487), P1N; N-terminal fragment of phot1 (1-619), P1C; C-terminal fragment of phot1 (620-996).”
Self-citationThe Control of Transpiration. Insights from Arabidopsis
Nilson, S. E., & Assmann, S. M. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.106.093161 · Cited by 225 · see citing works
“Studies that assess impacts of light (Kinoshita et al., 2001; Sothern et al., 2002), CO2 (Hashimoto et al., 2006; Teng et al., 2006; Young et al., 2006), and humidity (Assmann et al., 2000; Yoshida et al., 2002; Xie et al., 2006) on transpiration, while not discussed here, are equally important to…”
BackgroundGuard cells: a dynamic signaling model
Fan, L.-M., Zhao, Z., & Assmann, S. M. (2004) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2004.07.009 · Cited by 226 · see citing works
“The blue-light response is mediated to a great extent by phototropins, with possible contributions from zeaxanthin or phytochrome under specialized conditions [52,53].”
Guard cell metabolism and CO2 sensing
Vavasseur, A., & Raghavendra, A. S. (2005) · New Phytologist · doi:10.1111/j.1469-8137.2004.01276.x · Cited by 222 · see citing works
“Recently the blue light receptor was determined (Kinoshita et al., 2001).”
Sirichandra, C., Wasilewska, A., Vlad, F., Valon, C., & Leung, J. (2009) · Journal of Experimental Botany · doi:10.1093/jxb/ern340 · Cited by 218 · see citing works
“Both are critical for blue-light stimulation of stomatal opening as the double mutant phot1,phot2—but not their respective single mutants—is completely insensitive to blue light (Kinoshita et al., 2001).”
BackgroundPrimary Reactions of the LOV2 Domain of Phototropin, a Plant Blue-Light Photoreceptor
Kennis, J. T. M., Crosson, S., Gauden, M., van Stokkum, I. H. M., Moffat, K., & van Grondelle, R. (2003) · Biochemistry · doi:10.1021/bi034022k · Cited by 221 · see citing works
Ohgishi, M., Saji, K., Okada, K., & Sakai, T. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0305984101 · Cited by 215 · see citing works
Phototropism: Growing towards an Understanding of Plant Movement
Liscum, E., Askinosie, S. K., Leuchtman, D. L., Morrow, J., Willenburg, K. T., & Coats, D. R. (2014) · The Plant Cell · doi:10.1105/tpc.113.119727 · Cited by 215 · see citing works
Inada, S., Ohgishi, M., Mayama, T., Okada, K., & Sakai, T. (2004) · The Plant Cell · doi:10.1105/tpc.019901 · Cited by 215 · see citing works
“Kinoshita et al. (2001) showed that phot1 and phot2 function redundantly in stomatal opening to blue light irradiation.”
MethodInfluentialLight perception and signalling in higher plants
Gyula, P., Schäfer, E., & Nagy, F. (2003) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(03)00082-7 · Cited by 217 · see citing works
“these receptors with different partners — for example, Hþ-ATPase in guard cells [8], ion transporters or channel proteins in other leaf cells [40], and maybe auxin transporters in stem cells — result in different movement responses in different parts of the plant.”
BackgroundDegradation of Phytochrome Interacting Factor 3 in Phytochrome-Mediated Light Signaling
Park, E., Kim, J.-H., Lee, Y. J., Shin, J., Oh, E., Chung, W., Liu, J. R., & Choi, G. (2004) · Plant and Cell Physiology · doi:10.1093/pcp/pch125 · Cited by 215 · see citing works
Huang, K., & Beck, C. F. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0931459100 · Cited by 210 · see citing works
LOV Domain-Containing F-Box Proteins: Light-Dependent Protein Degradation Modules in Arabidopsis
Ito, S., Song, Y. H., & Imaizumi, T. (2012) · Molecular Plant · doi:10.1093/mp/sss013 · Cited by 211 · see citing works
“…phototropism (Sakai et al., 2001), chloroplast relocation movement (Kagawa et al., 2001; Sakai et al., 2001), light-induced stomatal opening (Kinoshita et al., 2001), cotyledon and leaf expansion (Sakamoto and Briggs, 2002; Takemiya et al., 2005), and hypocotyl growth (Folta and Spalding,…”
BackgroundFLOWERING LOCUS T Regulates Stomatal Opening
Kinoshita, T., Ono, N., Hayashi, Y., Morimoto, S., Nakamura, S., Soda, M., Kato, Y., Ohnishi, M., Nakano, T., Inoue, S., et al. (2011) · Current Biology · doi:10.1016/j.cub.2011.06.025 · Cited by 206 · see citing works
Self-citationMacedo, A. F., Leal-Costa, M. V., Tavares, E. S., Lage, C. L. S., & Esquibel, M. A. (2010) · Environmental and Experimental Botany · doi:10.1016/j.envexpbot.2010.05.012 · Cited by 202 · see citing works
The signal transducing photoreceptors of plants
Franklin, K. A., Larner, V. S., & Whitelam, G. C. (2005) · The International Journal of Developmental Biology · doi:10.1387/ijdb.051989kf · Cited by 202 · see citing works
“Whereas single (phot1, phot2 ) mutants displayed increased stomatal aperture in response to blue light, the phot1phot2 double mutant remained unresponsive (Kinoshita et al., 2001).”
BackgroundChoi, H. G., Moon, B. Y., & Kang, N. J. (2015) · Scientia Horticulturae · doi:10.1016/j.scienta.2015.03.022 · Cited by 201 · see citing works
Sang, Y., Li, Q., Rubio, V., Zhang, Y., Mao, J., Deng, X., & Yang, H. (2005) · The Plant Cell · doi:10.1105/tpc.104.029645 · Cited by 201 · see citing works
“, 2001) and blue light–induced stomatal opening (Kinoshita et al., 2001), has also been shown to dimerize through its LOV1 domain (Salomon et al.”
BackgroundLi, H., Tang, C., & Xu, Z. (2012) · Scientia Horticulturae · doi:10.1016/j.scienta.2012.10.009 · Cited by 200 · see citing works
Haberer, G., Hindemitt, T., Meyers, B. C., & Mayer, K. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.046466 · Cited by 197 · see citing works
“In Arabidopsis, partial redundancy and overlapping functionality for duplicated genes (e.g. SHATTERPROOF 1 and 2, AP1/CAULIFLOWER, PHOT1 and 2) have been reported (Ferrandiz et al., 2000; Liljegren et al., 2000; Kinoshita et al., 2001; Pinyopich et al., 2003).”
BackgroundYang, X., Hu, R., Yin, H., Jenkins, J. W., Shu, S., Tang, H., Liu, D., Weighill, D. A., Yim, W. C., Ha, J., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01491-7 · Cited by 198 · see citing works
Common and unique elements of the ABA-regulated transcriptome of Arabidopsis guard cells
Wang, R., Pandey, S., Song, L., Gookin, T. E., Zhao, Z., Albert, R., & Assmann, S. M. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-216 · Cited by 196 · see citing works
“CRY1/BLU1 (AT4G08920) encodes the blue light photoreceptor cryptochrome 1 and has been reported to participate in blue light-regulation of stomatal movements [72], while NPH3 functions downstream of the PHOT1/PHOT2 blue light photoreceptors which mediate blue light-specific stomatal opening [73].”
BackgroundZhang, M., Yin, W., Chen, X., Xu, F., Ding, M., Ye, W., Kawai, Y., Toda, Y., Hayashi, Y., Suzuki, T., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-20964-4 · Cited by 194 · see citing works
Self-citationFolta, K. M., & Childers, K. S. (2008) · HortScience · doi:10.21273/hortsci.43.7.1957 · Cited by 192 · see citing works
Regulation of Transpiration to Improve Crop Water Use
Yoo, C. Y., Pence, H. E., Hasegawa, P. M., & Mickelbart, M. V. (2009) · Critical Reviews in Plant Sciences · doi:10.1080/07352680903173175 · Cited by 190 · see citing works
“PHOTOTROPIN 1 and 2 (PHOT1 and PHOT2) are serine/threonine protein kinases that function as blue-light receptors for stomatal opening (Kinoshita et al., 2001).”
BackgroundHarada, A., Sakai, T., & Okada, K. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1336802100 · Cited by 185 · see citing works
OnGuard, a Computational Platform for Quantitative Kinetic Modeling of Guard Cell Physiology
Hills, A., Chen, Z., Anna Amtmann, A., Blatt, M. R., & Lew, V. L. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.197244 · Cited by 184 · see citing works
“…or 20% of their outputs in the Open Reference State, consistent with experimental estimates of the known light-stimulated activities of plasma membrane ATPases (Assmann et al., 1985; Shimazaki et al., 1986; Serrano et al., 1988; Goh et al., 1995, 1996; Kinoshita et al., 2001; Chen et al., 2012).”
Background
- Authors
- Kinoshita, T., Doi, M., Suetsugu, N., Kagawa, T., Wada, M., & Shimazaki, K.-I.
- Affiliations
- Kyushu University (JP)
- National Institute for Basic Biology (JP)
- Corresponding author
- Shimazaki, Ken-ichiro
- Venue
- Nature
- Published
- 2001-12
- Volume
- 414
- Issue
- 6864
- Pages
- 656-660
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2036131768
- Cited by
- 899
- References
- 31
- Citations by year
- 2026: 24 · 2025: 27 · 2024: 45 · 2023: 31 · 2022: 43 · 2021: 42 · 2020: 40 · 2019: 42 · 2018: 40 · 2017: 33 · 2016: 37 · 2015: 34 · 2014: 43 · 2013: 33 · 2012: 42
- FWCI
- 45.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Photosynthetic Processes and Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Photoreceptor and optogenetics research
- Keywords
- phot1, phot2, blue light receptor, stomatal opening, guard cells, Arabidopsis thaliana, cryptochrome, plasma membrane H+-ATPase, potassium accumulation, zeaxanthin, phototropism
- MeSH terms
- Cell Membrane, Proton-Translocating ATPases, Light, Mutation, Phosphoproteins, Protein Serine-Threonine Kinases, Arabidopsis, Plant Epidermis, Reverse Transcriptase Polymerase Chain Reaction, Arabidopsis Proteins, Photosynthetic Reaction Center Complex Proteins
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