Taiwan–Japan Plant Biology 2017 Spotlight Issue: From Light Signals/Signaling to Photosynthesis and Chloroplast Development

Taiwan–Japan Plant Biology 2017 Spotlight Issue: From Light Signals/Signaling to Photosynthesis... The Taiwan–Japan Plant Biology 2017 (TJPB2017) conference was held on November 3–6, 2017 at the Academia Sinica in Taipei, Taiwan. This was the first joint meeting of the Taiwan Society of Plant Biologists (TSPB) and the Japanese Society of Plant Physiologists (JSPP), and brought together 680 plant researchers to share and discuss their latest scientific discoveries over the two and a half days packed with six keynote presentations, 71 invited talks, 73 short talks and 350 poster presentations (Fig. 1). Both the TSPB and JSPP were established in the late 1950s to promote communication between members engaged or interested in diverse plant research fields, ranging from basic science, to applied agriculture and pharmacology. The two societies share common interests and historical backgrounds in plant sciences, and for years sought the opportunity to strengthen their academic interactions, discussions and collaborations. They finally realized the organization of this joint meeting, which took place as an extension of the TSPB annual meeting, and a satellite meeting of the JSPP annual meeting. The scientific organizers were Ming-Tsair Chan (Academia Sinica, Taiwan) from the TSPB and Wataru Sakamoto (Okayama University, Japan) from the JSPP. Fig. 1 View largeDownload slide A group photograph taken in front of the Humanities and Social Science Building, Academia Sinica, Taipei. Fig. 1 View largeDownload slide A group photograph taken in front of the Humanities and Social Science Building, Academia Sinica, Taipei. The TJPB2017 opened with a keynote talk by Tetsuya Higashiyama (Nagoya University, Japan), who presented his group’s work on plant reproduction using state-of-the-art live-cell imaging techniques. The second day of the meeting featured two other keynote speakers: Jun Minagawa (National Institute for Basic Biology, Japan), who presented his recent studies on photosynthesis regulation focusing on excess light acclimation mechanisms in green algae; and Shyi-Dong Yeh (National Chung Hsing University, Taiwan), who introduced cross-protection strategies to control the serious papaya ring spot disease in Taiwan. The final three keynote talks were held on the last day of the meeting. John Bowman (Monash University, Australia) discussed the evolution and diversification of key transcription factors regulating the life cycle of early plant lineages. Erich Grotewold (Michigan State University, USA) fascinated the audience with his work on novel gene regulatory networks controlling maize metabolism by looking at multiple transcription factors and genomic loci using high-throughput chromatin immunoprecipitation-sequencing and yeast one-hybrid approaches. Finally, at the closing session, Tzyy-Jen Chiou (Academia Sinica, Taiwan) presented recent progress on microRNA-mediated regulatory mechanisms for inorganic phosphate uptake, transition and storage. The TJPB2017 meeting covered a broad spectrum of plant research, with 15 oral sessions by invited speakers, and a number of selected 5 min short talks. The session topics included environmental responses, biomembranes, ion/solute transporters, organelles, plant–microbe interactions, evolution, taxonomy, photoresponses, clock, phytohormones, membrane trafficking, cell walls, photosynthesis, vegetative growth, cell cycle/division, transcriptional/post-transcriptional regulation, epigenetics, protein modification, proteolysis, reproductive growth, flowering, primary metabolism, secondary metabolism, ecophysiology, bioresources and emerging technologies. Great advances have recently been made in understanding how plants perceive and utilize light signals and energy for chloroplast function and whole-organism physiology. For the purpose of this Spotlight Issue, we will further explore three of the sessions at the TJPB2017 based on this theme, namely on light signaling, photosynthesis and chloroplast development. Phytochrome and Cryptochrome: Beyond the Regulation of Transcription Factors For plants, light not only serves as the energy source for photosynthesis but is also an important environmental signal for adaptation. Plants perceive light signals using several photoreceptors, such as the red/far-red light-absorbing phytochrome and the blue light-absorbing cryptochrome, and control gene expression to modulate their morphology and metabolism in response to light. For example, various aspects of photosynthesis and chloroplast development are known to be regulated by these photoreceptors (Berry et al. 2013). Session 6 ‘Photoreceptors, Photoresponses/Clock’, held on day 2 of the meeting, included four selected short talks by emerging young scientists in the field: Guan-Hong Chen (Academia Sinica, Taiwan), Shao-li Yang (National Taiwan University, Taiwan), Norihito Nakamichi (Nagoya University, Japan) and Gen-Jen Jang (Academia Sinica, Taiwan). Four invited speakers also presented cutting-edge research during this session. The first looked at transcriptional regulation by phytochromes and chyroptochromes, which regulate the activity of several transcription factors and can induce genome-wide transcriptional changes at target loci (Galvão and Fankhauser 2015). Recently, however, Shih-Long Tu (Academia Sinica, Taiwan) and colleagues performed mRNA-seq analysis in the moss Physcomitrella and found that phytochromes control not only transcription but also alternative splicing at a similar genomic scale (Wu et al. 2014). This observation was confirmed in Arabidopsis (Shikata et al. 2014), suggesting that phytochrome-mediated alternative splicing control is widely conserved in plants. Tu’s group is now elucidating the molecular mechanism of this regulation, and their recent progress together with data emerging from other groups is reviewed in this issue by Cheng and Tu (2018). Tomonao Matsushita (Kyushu University, Japan) presented his group’s latest surprising discovery that phytochrome impacts yet another aspect of gene expression. Through intensive transcription start site sequencing (TSS-seq) analysis, they found that phytochrome directly induced the selection of alternative promoters in >2,000 genes in Arabidopsis, resulting in light-dependent production of protein isoforms with different subcellular localizations (Ushijima et al. 2017; Fig. 2). Furthermore, they provided physiological evidence to demonstrate that this mechanism allows plants to respond metabolically to fluctuating light conditions, resulting in more efficient photosynthesis (Ushijima et al. 2017). These results not only show that alternative promoter usage constitutes a fundamental mechanism by which plants can adapt to different light environments, but also reveal a significant additional layer in the universal mechanism regulating eukaryotic gene expression. Fig. 2 View largeDownload slide Phytochromes induce genome-wide alterations in alternative promoter selection, to control protein subcellular localization in response to changing light conditions. The figure is adapted from Ushijima et al. (2017) with permission from the publisher. Fig. 2 View largeDownload slide Phytochromes induce genome-wide alterations in alternative promoter selection, to control protein subcellular localization in response to changing light conditions. The figure is adapted from Ushijima et al. (2017) with permission from the publisher. Additional studies have shown that cryptochromes and phytochromes substantially share the same downstream components to mediate similar light responses in plants, despite having completely different evolutionary origins (Galvão and Fankhauser 2015). However, Yoshito Oka’s group at the Fujian Agriculture and Forestry University in China have recently found that cryptochromes also possess a unique desensitizing mechanism utilizing the specific factor BIC1, which inhibits dimerization of the cryptochrome molecules (Wang et al. 2016). Since plant cryptochromes are now extensively used as optogenetic tools in animal cells (Shcherbakova et al. 2015), BIC1 is likely to confer a more precise and sophisticated control of cryptochrome-mediated optogenetic systems in various biological processes. The circadian clock is also an important target of light signaling control in plants; photoreceptors such as phytochrome and cryptochrome input the ambient light signal to reset the circadian clock for optimal photosynthesis and growth. Shu-Hsing Wu (Academia Sinica, Taiwan) gave a very insightful talk on the recent molecular analysis of LWD1, a clock protein initially identified by her group as a novel light-responsive gene (Wu et al. 2008). LWD1 associates with the promoter region of CCA1, a major component of the central oscillator, by directly binding to TCP transcription factors, and thereby acts as a co-activator of CCA1 to sustain the robust rhythm of its expression (Wu et al. 2016). Photosynthetic Electron Flow and Chloroplast Biogenesis Session 9 ‘Photosynthesis, environmental response of photosynthesis and respiration’ included four short talks selected from poster presentations by: Helena Sapeta (Hokkaido University, Japan), Ting-Hung Lin (Academia Sinica, Taiwan), Satomi Takeda (Osaka Prefecture University, Japan) and Yusuke Kato (Okayama University, Japan). These were preceded by four talks focusing on various aspects of photosynthesis and chloroplast biology. Toshiharu Shikanai (Kyoto University, Japan) kicked off the session with a presentation on the structure of the chloroplast NDH–PSI supercomplex. The chloroplast NADH dehydrogenase-like (NDH) complex mediates an alternative cyclic electron transport around PSI by recycling electrons from ferredoxin to the plastoquinone pool. Along with another cyclic route mediated by PGR5/PGRL1, the NDH complex finely regulates the proton motive force across the thylakoid membrane. NDH associates with two copies of the PSI supercomplex consisting of the PSI core and four light-harvesting complex I (LHCI) proteins via two additional LHCI proteins, Lhca5 and Lhca6, which act as linkers. Assembly of the PSI supercomplex is required for the full assembly and stability of the NDH complex (Kato et al. 2018), especially under high light intensities. Based on biochemical and genetic evidence, the structure of the NDH–PSI supercomplex has recently been proposed (Otani et al. 2017, Otani et al. 2018). The second invited talk by Hsiu-An Chu (IPMB/Academica Sinica, Taiwan) presented a novel plastoquinone (Qc), which is attached to PSII in cyanobacteria. Qc was discovered from the crystal structure of PSII isolated from Thermosynechococcus elongatus. To determine its function, a series of mutations were introduced into cytochrome b559 and PsbJ proteins in Synechocystis sp. PCC6803 at positions surrounding the Qc site and those forming the diffusion channel of plastoquinone. In the mutants, PSII was assembled normally, but two regulatory mechanisms of light-harvesting, i.e. state transitions and orange carotenoid protein-dependent energy dissipation, were altered. Unexpectedly, some mutant lines showed enhanced growth rates compared with wild-type cyanobacteria, possibly due to the manipulation of photoprotection mechanisms. It has been proposed that the Qc site may sense the redox state of the plastoquinone pool to modulate short-term light responses in cyanobacteria (J.Y. Huang et al. 2016b) Masato Nakai (Osaka University, Japan) presented the latest results from his group on the molecular mechanisms of chloroplast protein import and their curious evolutionary history. The import of proteins from the cytosol to the chloroplast stroma requires two translocons, one localized in the outer envelope (TOC) and one in the inner envelop (TIC). In 2013, the group of Masato Nakai reported the isolation of a 1 MDa complex from the inner envelope of chloroplasts in Arabidopsis (Kikuchi et al. 2013). His group discovered that this large complex surprisingly included the Tic214 protein, encoded by the largest open reading frame (ycf1) in the chloroplast genome. Even more intriguingly, some phototrophs including glaucophyta, rhodophyta and also grasses lack this ‘green’ TIC and instead possess a ‘non-photosynthetic type’ or ‘ancestral type’ of TIC (Nakai 2015). This topic is extensively reviewed by Nakai (2018) in this issue. Finally, Yee-yung Charng (Academia Sinica, Taiwan) talked about the chlorophyll salvage cycle and its role in photosynthesis. During leaf senescence, chlorophyll a breakdown is initiated by the removal of magnesium (Mg) by SGR (Mg-dechelatase), and the resulting pheophytin a is then dephytilated by PPH (pheophytinase). The Arabidopsis cld1-1 (chlorophyll dephytylase1) mutant is sensitive to heat shock and has a missense mutation in the gene encoding an α/β-hydrolase superfamily protein (CLD1), which shares the conserved motif with PPH and localizes to chloroplasts. Although the substrate of PPH is pheophytin a, recombinant CLD1 dephytylates chlorophylls a/b and pheophytin a. Unlike PPH, CLD1 is mainly expressed in green leaves but not during senescence. Together with chlorophyll synthase (CHLG), CLD1 forms the salvage cycle of chlorophylls Active repair of the PSII reaction center is accompanied by this turnover of chlorophylls This contrasts with the function of SGR/PPH in chlorophyll breakdown during senescence (Lin et al. 2016). Chloroplasts and Mitochondria: Endosymbiotic Organelles Requiring Co-ordinated Regulation in Biogenesis and Homeostasis Session 3 ‘Organelles and cytoskeletons’, chaired by Hsou-min Li (Academia Sinica, Taiwan) and Wataru Sakamoto, centered on the functions, dynamics and biogenesis of intracellular structures and organelles; in particular mitochondria and chloroplasts. These two organelles emerged independently in plant cells through endosymbiosis and play central roles in many aspects of cellular function, metabolism and homeostasis. Insights into the similarities and differences between these organelles will guide us to further understand their development and impact on plant physiology. Plant chloroplasts and mitochondria both retain their own genomes of bacterial origins, which are present in multiple copies and encode limited, yet essential, subsets of the respective intraorganellar proteins. The genome copy number of these organelles is variable and dependent on cellular contexts, but the mechanism(s) determining the quantity of organelle genomes remain unclear. Sakamoto employed a microscopy-based forward genetics approach to screen for Arabidopsis mutants with aberrant organellar genome accumulation in pollen, and identified DPD1 as a conserved exonuclease functioning in plastids and mitochondria (Matsushima et al. 2011). DPD1 expression is development-dependent and tissue-specific with the highest expression levels observed in senescing leaves (Tang and Sakamoto 2011, Sakamoto and Takami 2014). The possible function of DPD1 during leaf senescence was discussed. An overview of quality control of chloroplast DNA is further reviewed in this issue (see Sakamoto and Takami 2018). Neither plastids nor mitochondria are obtained from de novo biogenesis (Arimura 2018). Instead, their biogenesis and modes require growth and division of pre-existing organelles. In the case of mitochondria, their size, number, structure, shape and morphology are dynamic in the plant lineage; these are conferred through recurring fission and fusion events, though the molecular basis underlying their regulation is not fully understood. Shin-ichi Arimura (University of Tokyo, Japan) presented data showing the means by which mitochondrial fission is controlled in Arabidopsis and liverworts. Mitochondrial fission in the model eukaryote Saccharomyces cerevisiae requires the cytosolic dynamin-related GTPase Dnm1p to be recruited to mitochondrial fission sites through interaction with the outer membrane protein Fis1p and the adaptor proteins Mdv1p/Caf4p (Bui and Shaw 2013). In plants, dynamin recruitment to the fission sites involves the plant-specific ELM1 proteins. While Fis1p homologs that localize to mitochondria have been reported, they are unlikely to play a pivotal role in plant mitochondrial fission (Nagaoka et al. 2017, Arimura 2018). Similar to chloroplasts, plant mitochondria also function in regulating metabolic and energetic homeostasis, with mitochondrial dysfunction causing deleterious effects on plant growth and development. Ming-Hsiun Hsieh (Academia Sinica, Taiwan) presented his work on slow growth (slo) mutants in Arabidopsis and on the identification of the responsible genes including SLO1, which encodes an E motif-containing pentatricopeptide repeat (PPR) protein participating in mitochondrial RNA editing of NADH dehydrogenase subunits 4 and 9 (nad4/9) (Sung et al. 2010), and SLO3, which codes for a P-type PPR protein specifically involved in intron splicing of the nad7 transcript in mitochondria (Hsieh et al. 2015). The results presented suggest important roles for the PPR proteins in post-transcriptional regulation of mitochondrial RNA metabolism. The majority of the chloroplast proteome is nuclear encoded, and thus synthesized in the cytosol as precursor proteins with an N-terminal cleavable target peptide to navigate them to the translocation channels located on the chloroplast envelopes for import. The ATP requirement for protein import suggested the presence of an ATP-dependent motor machinery that could pull on pre-proteins as they pass through the channels (Pain and Blobel 1987). Several ATPase chaperones, including stromal cpHsc70 and Hsp93, could associate with the translocation machinery, but whether and how these chaperones function in protein import is unclear. Li showed that Hsp93 directly binds to pre-proteins at the transit peptide and mature domains, whereas cpHsc70 associates with pre-proteins and processed proteins (P.K. Huang et al. 2016a), suggesting their distinct but partially overlapping functions during protein import. Following these four invited talks, a further six short talks were given by the poster presentation award winners: Masanori Izumi (Tohoku University, Japan), Kenji Nishimura (Okayama University, Japan), Kana Kishimoto (Kumamoto University, Japan), Kosei Iwabuchi (Konan University, Japan), Chiung-Chih Chu (Academia Sinica, Taiwan) and Mari Takusagawa (Kyoto University, Japan). In this Spotlight Issue, the Li group review recent findings about the role of galactolipids in plant development, which are essential constituents of chloroplast membranes (Li and Yu 2018). Another recent finding on chlorophagy, a selective degradation of damaged chloroplasts, is also reviewed (Nakamura and Izumi 2018). Perspectives Light signaling, photosynthesis and chloroplast development are closely entwined. Significant progress has been made in the past few years to understand the regulation of these cellular processes. In particular, a new layer of complexity in the control of the transcriptome through light signaling involving a phytochrome photoreceptor was recently discovered, opening a new dimension for studying photosynthesis and chloroplast development, as well as plant physiology and adaptation. The TJPB2017 successfully presented a bird’s-eye view of the broad spectrum of research topics connecting light signaling, photosynthesis and chloroplast biogenesis/homeostasis. Indeed, the rest of the TJPB2017 was also a huge success; the meeting program was full of top-quality science with some exciting, unpublished experimental data, new concepts and ideas, and the participants enjoyed discussing their research and making new acquaintances with others working in related or different fields of plant biology. The meeting also provided a great opportunity for students and young scientists to discuss and communicate their research externally. We greatly anticipate the next joint meeting (to be held in Japan) to further strengthen interactions between the TSPB and the JSPP. Acknowledgments We express our sincere thanks to the TSPB, especially to President Chang-Hsien Yang, Secretory General Jun-Yi Yang and the TJPB2017 committee members, for providing us with the opportunity to stimulate scientific exchange. K.N. is a post-doctoral fellow supported by the Japan Society for the Promotion of Science. Disclosures The authors have no conflicts of interest to declare. References Arimura S.I. ( 2018 ) Fission and fusion of plant mitochondria, and genome maintenance . Plant Physiol . 176 : 152 – 161 . Google Scholar CrossRef Search ADS PubMed Berry J.O. , Yerramsetty P. , Zielinski A.M. , Mure C.M. ( 2013 ) Photosynthetic gene expression in higher plants . Photosynth. Res . 117 : 91 – 120 . Google Scholar CrossRef Search ADS PubMed Bui H.T. , Shaw J.M. ( 2013 ) Dynamin assembly strategies and adaptor proteins in mitochondrial fission . Curr. Biol. 23 : R891 – R899 . Google Scholar CrossRef Search ADS PubMed Cheng Y.L. , Tu S.L. ( 2018 ) Plant Cell Physiol. 59: 1104–1110. Galvão V.C. , Fankhauser C. ( 2015 ) Sensing the light environment in plants: photoreceptors and early signaling steps . Curr. Opin. Neurobiol . 34 : 46 – 53 . Google Scholar CrossRef Search ADS PubMed Hsieh W.Y. , Liao J.C. , Chang C.Y. , Harrison T. , Boucher C. , Hsieh M.H. ( 2015 ) The SLOW GROWTH3 pentatricopeptide repeat protein is required for the splicing of mitochondrial NADH Dehydrogenase Subunit7 intron 2 in Arabidopsis . Plant Physiol. 168 : 490 – 501 . Google Scholar CrossRef Search ADS PubMed Huang J.Y. , Chiu Y.F. , Ortega J.M. , Wang H.T. , Tseng T.S. , Ke S.C. , et al. . ( 2016b ) Mutations of cytochrome b559 and PsbJ on and near the Qc site in photosystem II influence the regulation of short-term light response and photosynthetic growth of the cyanobacterium Synechocystis sp. PCC 6803 . Biochemistry 55 : 2214 – 2226 . Google Scholar CrossRef Search ADS Huang P.K. , Chan P.T. , Su P.H. , Chen L.J. , Li H.M. ( 2016a ) Chloroplast Hsp93 directly binds to transit peptides at an early stage of the preprotein import process . Plant Physiol. 170 : 857 – 866 . Google Scholar CrossRef Search ADS Kato Y. , Sugimoto K. , Shikanai T. ( 2018 ) NDH–PSI supercomplex assembly precedes full assembly of the NDH complex in chloroplast . Plant Physiol. 176 : 1728 – 1738 . Google Scholar CrossRef Search ADS PubMed Kikuchi S. , Bédard J. , Hirano M. , Hirabayashi Y. , Oishi M. , Imai M. , et al. . ( 2013 ) Uncovering the protein translocon at the chloroplast inner envelope membrane . Science 339 : 571 – 574 . Google Scholar CrossRef Search ADS PubMed Li H.M. , Yu C.W. 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( 2018 ) Plant Cell Physiol. 59: 1135–1143. Otani T. , Kato Y. , Shikanai T. ( 2018 ) Specific substitutions of light-harvesting complex I proteins associated with photosystem I are required for supercomplex formation with chloroplast NADH dehydrogenase-like complex . Plant J . 94 : 122 – 130 . Google Scholar CrossRef Search ADS PubMed Otani T. , Yamamoto H. , Shikanai T. ( 2017 ) Stromal loop of Lhca6 is responsible for the linker function required for the NDH–PSI supercomplex formation . Plant Cell Physiol . 58 : 851 – 861 . Google Scholar CrossRef Search ADS PubMed Pain D. , Blobel G. ( 1987 ) Protein import into chloroplasts requires a chloroplast ATPase . Proc. Natl. Acad. Sci. USA 84 : 3288 – 3292 . Google Scholar CrossRef Search ADS Sakamoto W. , Takami T. ( 2014 ) Nucleases in higher plants and their possible involvement in DNA degradation during leaf senescence . J. Exp. Bot . 65 : 3835 – 3843 . Google Scholar CrossRef Search ADS PubMed Sakamoto W. , Takami T. ( 2018 ) Plant Cell Physiol. 59: 1120–1127. Shcherbakova D.M. , Shemetov A.A. , Kaberniuk A.A. , Verkhusha V.V. ( 2015 ) Natural photoreceptors as a source of fluorescent proteins, biosensors, and optogenetic tools . Annu. Rev. Biochem. 84 : 519 – 550 . Google Scholar CrossRef Search ADS PubMed Shikata H. , Hanada K. , Ushijima T. , Nakashima M. , Suzuki Y. , Matsushita T. ( 2014 ) Phytochrome controls alternative splicing to mediate light responses in Arabidopsis . Proc. Natl. Acad. Sci. USA 111 : 18781 – 18786 . Google Scholar CrossRef Search ADS Sung T.Y. , Tseng C.C. , Hsieh M.H. ( 2010 ) The SLO1 PPR protein is required for RNA editing at multiple sites with similar upstream sequences in Arabidopsis mitochondria . Plant J . 63 : 499 – 511 . Google Scholar CrossRef Search ADS PubMed Tang L.Y. , Sakamoto W. ( 2011 ) Tissue-specific organelle DNA degradation mediated by DPD1 exonuclease . Plant Signal. Behav . 6 : 1391 – 1393 . Google Scholar CrossRef Search ADS PubMed Ushijima T. , Hanada K. , Gotoh E. , Yamori W. , Kodama Y. , Tanaka H. , et al. . ( 2017 ) Light controls protein localization through phytochrome-mediated alternative promoter selection . Cell 171 : 1316 – 1325 . Google Scholar CrossRef Search ADS PubMed Wang Q. , Zuo Z. , Wang X. , Gu L. , Yoshizumi T. , Yang Z. , et al. . ( 2016 ) Photoactivation and inactivation of Arabidopsis cryptochrome 2 . Science 354 : 343 – 347 . Google Scholar CrossRef Search ADS PubMed Wu H.P. , Su Y.S. , Chen H.C. , Chen Y.R. , Wu C.C. , Lin W.D. , et al. . ( 2014 ) Genome-wide analysis of light-regulated alternative splicing mediated by photoreceptors in Physcomitrella patens . Genome Biol. 15 : R10. Google Scholar CrossRef Search ADS PubMed Wu J.F. , Tsai H.L. , Joanito I. , Wu Y.C. , Chang C.W. , Li Y.H. , et al. . ( 2016 ) LWD–TCP complex activates the morning gene CCA1 in Arabidopsis . Nat. Commun. 7 : 13181 . Google Scholar CrossRef Search ADS PubMed Wu J.F. , Wang Y. , Wu S.H. ( 2008 ) Two new clock proteins, LWD1 and LWD2, regulate Arabidopsis photoperiodic flowering . Plant Physiol . 148 : 948 – 959 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Plant and Cell Physiology Oxford University Press

Taiwan–Japan Plant Biology 2017 Spotlight Issue: From Light Signals/Signaling to Photosynthesis and Chloroplast Development

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Abstract

The Taiwan–Japan Plant Biology 2017 (TJPB2017) conference was held on November 3–6, 2017 at the Academia Sinica in Taipei, Taiwan. This was the first joint meeting of the Taiwan Society of Plant Biologists (TSPB) and the Japanese Society of Plant Physiologists (JSPP), and brought together 680 plant researchers to share and discuss their latest scientific discoveries over the two and a half days packed with six keynote presentations, 71 invited talks, 73 short talks and 350 poster presentations (Fig. 1). Both the TSPB and JSPP were established in the late 1950s to promote communication between members engaged or interested in diverse plant research fields, ranging from basic science, to applied agriculture and pharmacology. The two societies share common interests and historical backgrounds in plant sciences, and for years sought the opportunity to strengthen their academic interactions, discussions and collaborations. They finally realized the organization of this joint meeting, which took place as an extension of the TSPB annual meeting, and a satellite meeting of the JSPP annual meeting. The scientific organizers were Ming-Tsair Chan (Academia Sinica, Taiwan) from the TSPB and Wataru Sakamoto (Okayama University, Japan) from the JSPP. Fig. 1 View largeDownload slide A group photograph taken in front of the Humanities and Social Science Building, Academia Sinica, Taipei. Fig. 1 View largeDownload slide A group photograph taken in front of the Humanities and Social Science Building, Academia Sinica, Taipei. The TJPB2017 opened with a keynote talk by Tetsuya Higashiyama (Nagoya University, Japan), who presented his group’s work on plant reproduction using state-of-the-art live-cell imaging techniques. The second day of the meeting featured two other keynote speakers: Jun Minagawa (National Institute for Basic Biology, Japan), who presented his recent studies on photosynthesis regulation focusing on excess light acclimation mechanisms in green algae; and Shyi-Dong Yeh (National Chung Hsing University, Taiwan), who introduced cross-protection strategies to control the serious papaya ring spot disease in Taiwan. The final three keynote talks were held on the last day of the meeting. John Bowman (Monash University, Australia) discussed the evolution and diversification of key transcription factors regulating the life cycle of early plant lineages. Erich Grotewold (Michigan State University, USA) fascinated the audience with his work on novel gene regulatory networks controlling maize metabolism by looking at multiple transcription factors and genomic loci using high-throughput chromatin immunoprecipitation-sequencing and yeast one-hybrid approaches. Finally, at the closing session, Tzyy-Jen Chiou (Academia Sinica, Taiwan) presented recent progress on microRNA-mediated regulatory mechanisms for inorganic phosphate uptake, transition and storage. The TJPB2017 meeting covered a broad spectrum of plant research, with 15 oral sessions by invited speakers, and a number of selected 5 min short talks. The session topics included environmental responses, biomembranes, ion/solute transporters, organelles, plant–microbe interactions, evolution, taxonomy, photoresponses, clock, phytohormones, membrane trafficking, cell walls, photosynthesis, vegetative growth, cell cycle/division, transcriptional/post-transcriptional regulation, epigenetics, protein modification, proteolysis, reproductive growth, flowering, primary metabolism, secondary metabolism, ecophysiology, bioresources and emerging technologies. Great advances have recently been made in understanding how plants perceive and utilize light signals and energy for chloroplast function and whole-organism physiology. For the purpose of this Spotlight Issue, we will further explore three of the sessions at the TJPB2017 based on this theme, namely on light signaling, photosynthesis and chloroplast development. Phytochrome and Cryptochrome: Beyond the Regulation of Transcription Factors For plants, light not only serves as the energy source for photosynthesis but is also an important environmental signal for adaptation. Plants perceive light signals using several photoreceptors, such as the red/far-red light-absorbing phytochrome and the blue light-absorbing cryptochrome, and control gene expression to modulate their morphology and metabolism in response to light. For example, various aspects of photosynthesis and chloroplast development are known to be regulated by these photoreceptors (Berry et al. 2013). Session 6 ‘Photoreceptors, Photoresponses/Clock’, held on day 2 of the meeting, included four selected short talks by emerging young scientists in the field: Guan-Hong Chen (Academia Sinica, Taiwan), Shao-li Yang (National Taiwan University, Taiwan), Norihito Nakamichi (Nagoya University, Japan) and Gen-Jen Jang (Academia Sinica, Taiwan). Four invited speakers also presented cutting-edge research during this session. The first looked at transcriptional regulation by phytochromes and chyroptochromes, which regulate the activity of several transcription factors and can induce genome-wide transcriptional changes at target loci (Galvão and Fankhauser 2015). Recently, however, Shih-Long Tu (Academia Sinica, Taiwan) and colleagues performed mRNA-seq analysis in the moss Physcomitrella and found that phytochromes control not only transcription but also alternative splicing at a similar genomic scale (Wu et al. 2014). This observation was confirmed in Arabidopsis (Shikata et al. 2014), suggesting that phytochrome-mediated alternative splicing control is widely conserved in plants. Tu’s group is now elucidating the molecular mechanism of this regulation, and their recent progress together with data emerging from other groups is reviewed in this issue by Cheng and Tu (2018). Tomonao Matsushita (Kyushu University, Japan) presented his group’s latest surprising discovery that phytochrome impacts yet another aspect of gene expression. Through intensive transcription start site sequencing (TSS-seq) analysis, they found that phytochrome directly induced the selection of alternative promoters in >2,000 genes in Arabidopsis, resulting in light-dependent production of protein isoforms with different subcellular localizations (Ushijima et al. 2017; Fig. 2). Furthermore, they provided physiological evidence to demonstrate that this mechanism allows plants to respond metabolically to fluctuating light conditions, resulting in more efficient photosynthesis (Ushijima et al. 2017). These results not only show that alternative promoter usage constitutes a fundamental mechanism by which plants can adapt to different light environments, but also reveal a significant additional layer in the universal mechanism regulating eukaryotic gene expression. Fig. 2 View largeDownload slide Phytochromes induce genome-wide alterations in alternative promoter selection, to control protein subcellular localization in response to changing light conditions. The figure is adapted from Ushijima et al. (2017) with permission from the publisher. Fig. 2 View largeDownload slide Phytochromes induce genome-wide alterations in alternative promoter selection, to control protein subcellular localization in response to changing light conditions. The figure is adapted from Ushijima et al. (2017) with permission from the publisher. Additional studies have shown that cryptochromes and phytochromes substantially share the same downstream components to mediate similar light responses in plants, despite having completely different evolutionary origins (Galvão and Fankhauser 2015). However, Yoshito Oka’s group at the Fujian Agriculture and Forestry University in China have recently found that cryptochromes also possess a unique desensitizing mechanism utilizing the specific factor BIC1, which inhibits dimerization of the cryptochrome molecules (Wang et al. 2016). Since plant cryptochromes are now extensively used as optogenetic tools in animal cells (Shcherbakova et al. 2015), BIC1 is likely to confer a more precise and sophisticated control of cryptochrome-mediated optogenetic systems in various biological processes. The circadian clock is also an important target of light signaling control in plants; photoreceptors such as phytochrome and cryptochrome input the ambient light signal to reset the circadian clock for optimal photosynthesis and growth. Shu-Hsing Wu (Academia Sinica, Taiwan) gave a very insightful talk on the recent molecular analysis of LWD1, a clock protein initially identified by her group as a novel light-responsive gene (Wu et al. 2008). LWD1 associates with the promoter region of CCA1, a major component of the central oscillator, by directly binding to TCP transcription factors, and thereby acts as a co-activator of CCA1 to sustain the robust rhythm of its expression (Wu et al. 2016). Photosynthetic Electron Flow and Chloroplast Biogenesis Session 9 ‘Photosynthesis, environmental response of photosynthesis and respiration’ included four short talks selected from poster presentations by: Helena Sapeta (Hokkaido University, Japan), Ting-Hung Lin (Academia Sinica, Taiwan), Satomi Takeda (Osaka Prefecture University, Japan) and Yusuke Kato (Okayama University, Japan). These were preceded by four talks focusing on various aspects of photosynthesis and chloroplast biology. Toshiharu Shikanai (Kyoto University, Japan) kicked off the session with a presentation on the structure of the chloroplast NDH–PSI supercomplex. The chloroplast NADH dehydrogenase-like (NDH) complex mediates an alternative cyclic electron transport around PSI by recycling electrons from ferredoxin to the plastoquinone pool. Along with another cyclic route mediated by PGR5/PGRL1, the NDH complex finely regulates the proton motive force across the thylakoid membrane. NDH associates with two copies of the PSI supercomplex consisting of the PSI core and four light-harvesting complex I (LHCI) proteins via two additional LHCI proteins, Lhca5 and Lhca6, which act as linkers. Assembly of the PSI supercomplex is required for the full assembly and stability of the NDH complex (Kato et al. 2018), especially under high light intensities. Based on biochemical and genetic evidence, the structure of the NDH–PSI supercomplex has recently been proposed (Otani et al. 2017, Otani et al. 2018). The second invited talk by Hsiu-An Chu (IPMB/Academica Sinica, Taiwan) presented a novel plastoquinone (Qc), which is attached to PSII in cyanobacteria. Qc was discovered from the crystal structure of PSII isolated from Thermosynechococcus elongatus. To determine its function, a series of mutations were introduced into cytochrome b559 and PsbJ proteins in Synechocystis sp. PCC6803 at positions surrounding the Qc site and those forming the diffusion channel of plastoquinone. In the mutants, PSII was assembled normally, but two regulatory mechanisms of light-harvesting, i.e. state transitions and orange carotenoid protein-dependent energy dissipation, were altered. Unexpectedly, some mutant lines showed enhanced growth rates compared with wild-type cyanobacteria, possibly due to the manipulation of photoprotection mechanisms. It has been proposed that the Qc site may sense the redox state of the plastoquinone pool to modulate short-term light responses in cyanobacteria (J.Y. Huang et al. 2016b) Masato Nakai (Osaka University, Japan) presented the latest results from his group on the molecular mechanisms of chloroplast protein import and their curious evolutionary history. The import of proteins from the cytosol to the chloroplast stroma requires two translocons, one localized in the outer envelope (TOC) and one in the inner envelop (TIC). In 2013, the group of Masato Nakai reported the isolation of a 1 MDa complex from the inner envelope of chloroplasts in Arabidopsis (Kikuchi et al. 2013). His group discovered that this large complex surprisingly included the Tic214 protein, encoded by the largest open reading frame (ycf1) in the chloroplast genome. Even more intriguingly, some phototrophs including glaucophyta, rhodophyta and also grasses lack this ‘green’ TIC and instead possess a ‘non-photosynthetic type’ or ‘ancestral type’ of TIC (Nakai 2015). This topic is extensively reviewed by Nakai (2018) in this issue. Finally, Yee-yung Charng (Academia Sinica, Taiwan) talked about the chlorophyll salvage cycle and its role in photosynthesis. During leaf senescence, chlorophyll a breakdown is initiated by the removal of magnesium (Mg) by SGR (Mg-dechelatase), and the resulting pheophytin a is then dephytilated by PPH (pheophytinase). The Arabidopsis cld1-1 (chlorophyll dephytylase1) mutant is sensitive to heat shock and has a missense mutation in the gene encoding an α/β-hydrolase superfamily protein (CLD1), which shares the conserved motif with PPH and localizes to chloroplasts. Although the substrate of PPH is pheophytin a, recombinant CLD1 dephytylates chlorophylls a/b and pheophytin a. Unlike PPH, CLD1 is mainly expressed in green leaves but not during senescence. Together with chlorophyll synthase (CHLG), CLD1 forms the salvage cycle of chlorophylls Active repair of the PSII reaction center is accompanied by this turnover of chlorophylls This contrasts with the function of SGR/PPH in chlorophyll breakdown during senescence (Lin et al. 2016). Chloroplasts and Mitochondria: Endosymbiotic Organelles Requiring Co-ordinated Regulation in Biogenesis and Homeostasis Session 3 ‘Organelles and cytoskeletons’, chaired by Hsou-min Li (Academia Sinica, Taiwan) and Wataru Sakamoto, centered on the functions, dynamics and biogenesis of intracellular structures and organelles; in particular mitochondria and chloroplasts. These two organelles emerged independently in plant cells through endosymbiosis and play central roles in many aspects of cellular function, metabolism and homeostasis. Insights into the similarities and differences between these organelles will guide us to further understand their development and impact on plant physiology. Plant chloroplasts and mitochondria both retain their own genomes of bacterial origins, which are present in multiple copies and encode limited, yet essential, subsets of the respective intraorganellar proteins. The genome copy number of these organelles is variable and dependent on cellular contexts, but the mechanism(s) determining the quantity of organelle genomes remain unclear. Sakamoto employed a microscopy-based forward genetics approach to screen for Arabidopsis mutants with aberrant organellar genome accumulation in pollen, and identified DPD1 as a conserved exonuclease functioning in plastids and mitochondria (Matsushima et al. 2011). DPD1 expression is development-dependent and tissue-specific with the highest expression levels observed in senescing leaves (Tang and Sakamoto 2011, Sakamoto and Takami 2014). The possible function of DPD1 during leaf senescence was discussed. An overview of quality control of chloroplast DNA is further reviewed in this issue (see Sakamoto and Takami 2018). Neither plastids nor mitochondria are obtained from de novo biogenesis (Arimura 2018). Instead, their biogenesis and modes require growth and division of pre-existing organelles. In the case of mitochondria, their size, number, structure, shape and morphology are dynamic in the plant lineage; these are conferred through recurring fission and fusion events, though the molecular basis underlying their regulation is not fully understood. Shin-ichi Arimura (University of Tokyo, Japan) presented data showing the means by which mitochondrial fission is controlled in Arabidopsis and liverworts. Mitochondrial fission in the model eukaryote Saccharomyces cerevisiae requires the cytosolic dynamin-related GTPase Dnm1p to be recruited to mitochondrial fission sites through interaction with the outer membrane protein Fis1p and the adaptor proteins Mdv1p/Caf4p (Bui and Shaw 2013). In plants, dynamin recruitment to the fission sites involves the plant-specific ELM1 proteins. While Fis1p homologs that localize to mitochondria have been reported, they are unlikely to play a pivotal role in plant mitochondrial fission (Nagaoka et al. 2017, Arimura 2018). Similar to chloroplasts, plant mitochondria also function in regulating metabolic and energetic homeostasis, with mitochondrial dysfunction causing deleterious effects on plant growth and development. Ming-Hsiun Hsieh (Academia Sinica, Taiwan) presented his work on slow growth (slo) mutants in Arabidopsis and on the identification of the responsible genes including SLO1, which encodes an E motif-containing pentatricopeptide repeat (PPR) protein participating in mitochondrial RNA editing of NADH dehydrogenase subunits 4 and 9 (nad4/9) (Sung et al. 2010), and SLO3, which codes for a P-type PPR protein specifically involved in intron splicing of the nad7 transcript in mitochondria (Hsieh et al. 2015). The results presented suggest important roles for the PPR proteins in post-transcriptional regulation of mitochondrial RNA metabolism. The majority of the chloroplast proteome is nuclear encoded, and thus synthesized in the cytosol as precursor proteins with an N-terminal cleavable target peptide to navigate them to the translocation channels located on the chloroplast envelopes for import. The ATP requirement for protein import suggested the presence of an ATP-dependent motor machinery that could pull on pre-proteins as they pass through the channels (Pain and Blobel 1987). Several ATPase chaperones, including stromal cpHsc70 and Hsp93, could associate with the translocation machinery, but whether and how these chaperones function in protein import is unclear. Li showed that Hsp93 directly binds to pre-proteins at the transit peptide and mature domains, whereas cpHsc70 associates with pre-proteins and processed proteins (P.K. Huang et al. 2016a), suggesting their distinct but partially overlapping functions during protein import. Following these four invited talks, a further six short talks were given by the poster presentation award winners: Masanori Izumi (Tohoku University, Japan), Kenji Nishimura (Okayama University, Japan), Kana Kishimoto (Kumamoto University, Japan), Kosei Iwabuchi (Konan University, Japan), Chiung-Chih Chu (Academia Sinica, Taiwan) and Mari Takusagawa (Kyoto University, Japan). In this Spotlight Issue, the Li group review recent findings about the role of galactolipids in plant development, which are essential constituents of chloroplast membranes (Li and Yu 2018). Another recent finding on chlorophagy, a selective degradation of damaged chloroplasts, is also reviewed (Nakamura and Izumi 2018). Perspectives Light signaling, photosynthesis and chloroplast development are closely entwined. Significant progress has been made in the past few years to understand the regulation of these cellular processes. In particular, a new layer of complexity in the control of the transcriptome through light signaling involving a phytochrome photoreceptor was recently discovered, opening a new dimension for studying photosynthesis and chloroplast development, as well as plant physiology and adaptation. The TJPB2017 successfully presented a bird’s-eye view of the broad spectrum of research topics connecting light signaling, photosynthesis and chloroplast biogenesis/homeostasis. Indeed, the rest of the TJPB2017 was also a huge success; the meeting program was full of top-quality science with some exciting, unpublished experimental data, new concepts and ideas, and the participants enjoyed discussing their research and making new acquaintances with others working in related or different fields of plant biology. The meeting also provided a great opportunity for students and young scientists to discuss and communicate their research externally. We greatly anticipate the next joint meeting (to be held in Japan) to further strengthen interactions between the TSPB and the JSPP. Acknowledgments We express our sincere thanks to the TSPB, especially to President Chang-Hsien Yang, Secretory General Jun-Yi Yang and the TJPB2017 committee members, for providing us with the opportunity to stimulate scientific exchange. K.N. is a post-doctoral fellow supported by the Japan Society for the Promotion of Science. Disclosures The authors have no conflicts of interest to declare. References Arimura S.I. ( 2018 ) Fission and fusion of plant mitochondria, and genome maintenance . Plant Physiol . 176 : 152 – 161 . Google Scholar CrossRef Search ADS PubMed Berry J.O. , Yerramsetty P. , Zielinski A.M. , Mure C.M. ( 2013 ) Photosynthetic gene expression in higher plants . Photosynth. Res . 117 : 91 – 120 . Google Scholar CrossRef Search ADS PubMed Bui H.T. , Shaw J.M. 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Plant and Cell PhysiologyOxford University Press

Published: Apr 14, 2018

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