Chloroplast Photorelocation Movement: A Sophisticated Strategy for Chloroplasts to Perform Efficient Photosynthesis

Suetsugu, Noriyuki; Wada, Masamitsu

doi:10.5772/26838

Cited by 25 publications

(32 citation statements)

References 63 publications

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“…Although intensive observation of chloroplast photorelocation movement has been performed in diverse plant groups such as green algae, mosses, ferns, and seed plants since the 19th century (Senn, 1908;Suetsugu and Wada, 2012), knowledge of chloroplast photorelocation movement in liverworts is relatively limited. In this study, we observed light-induced movements of chloroplasts in M. polymorpha in detail.…”

Section: Phototropin-mediated Chloroplast Photorelocation Movements Imentioning

confidence: 99%

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Phototropin Encoded by a Single-Copy Gene Mediates Chloroplast Photorelocation Movements in the LiverwortMarchantia polymorpha

et al. 2014

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Blue-light-induced chloroplast photorelocation movement is observed in most land plants. Chloroplasts move toward weak-lightirradiated areas to efficiently absorb light (the accumulation response) and escape from strong-light-irradiated areas to avoid photodamage (the avoidance response). The plant-specific kinase phototropin (phot) is the blue-light receptor for chloroplast movements. Although the molecular mechanisms for chloroplast photorelocation movement have been analyzed, the overall aspects of signal transduction common to land plants are still unknown. Here, we show that the liverwort Marchantia polymorpha exhibits the accumulation and avoidance responses exclusively induced by blue light as well as specific chloroplast positioning in the dark. Moreover, in silico and Southern-blot analyses revealed that the M. polymorpha genome encodes a single PHOT gene, MpPHOT, and its knockout line displayed none of the chloroplast photorelocation movements, indicating that the sole MpPHOT gene mediates all types of movement. Mpphot was localized on the plasma membrane and exhibited blue-light-dependent autophosphorylation both in vitro and in vivo. Heterologous expression of MpPHOT rescued the defects in chloroplast movement of phot mutants in the fern Adiantum capillus-veneris and the seed plant Arabidopsis (Arabidopsis thaliana). These results indicate that Mpphot possesses evolutionarily conserved regulatory activities for chloroplast photorelocation movement. M. polymorpha offers a simple and versatile platform for analyzing the fundamental processes of phototropin-mediated chloroplast photorelocation movement common to land plants.

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Section: Phototropin-mediated Chloroplast Photorelocation Movements Imentioning

confidence: 99%

“…Molecular mechanisms for chloroplast photorelocation movements have been revealed through molecular genetic analyses using Arabidopsis (Suetsugu and Wada, 2012). The light-activated kinase phototropin was identified as the blue-light receptor (Jarillo et al, 2001;Kagawa et al, 2001;Sakai et al, 2001).…”

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Phototropin Encoded by a Single-Copy Gene Mediates Chloroplast Photorelocation Movements in the LiverwortMarchantia polymorpha

et al. 2014

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“…Both actin filaments and microtubules mediate these nuclear movements in animals and fungi, and the dynamics of these cytoskeletons or motor proteins generate the motive force (1,2). In sessile plants, chloroplasts (photosynthetic plastids) and nuclei change their intracellular positioning in response to light to adapt to fluctuating ambient light conditions, actions known as chloroplast and nuclear photorelocation movement, respectively (2,3).…”

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confidence: 99%

Actin-dependent plastid movement is required for motive force generation in directional nuclear movement in plants

Higa

Suetsugu

Kong

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Nuclear movement and positioning are indispensable for most cellular functions. In plants, strong light-induced chloroplast movement to the side walls of the cell is essential for minimizing damage from strong visible light. Strong light-induced nuclear movement to the side walls also has been suggested to play an important role in minimizing damage from strong UV light. Although both movements are regulated by the same photoreceptor, phototropin, the precise cytoskeleton-based force generation mechanism for nuclear movement is unknown, in contrast to the short actin-based mechanism of chloroplast movement. Here we show that actin-dependent movement of plastids attached to the nucleus is essential for lightinduced nuclear movement in the Arabidopsis leaf epidermal cell. We found that nuclei are always associated with some plastids, and that light-induced nuclear movement is correlated with the dynamics of short actin filaments associated with plastids. Indeed, nuclei without plastid attachments do not exhibit blue light-induced directional movement. Our results demonstrate that nuclei are incapable of autonomously moving in response to light, whereas attached plastids carry nuclei via the short actin filament-based movement. Thus, the close association between nuclei and plastids is essential for their cooperative movements and functions. P roper nuclear movement and positioning are essential for cellular function and organization, and defects in nuclear positioning cause impaired cellular development and diseases in animals, fungi, and plants (1, 2). Although nuclear positioning is essential primarily for determining the cell division plane, other functions of nuclear movement and positioning essential for normal development and cellular functions include directional movement and asymmetric positioning owing to internal causes or external stresses in nondividing G0 and/or G1 cells. Both actin filaments and microtubules mediate these nuclear movements in animals and fungi, and the dynamics of these cytoskeletons or motor proteins generate the motive force (1, 2). In sessile plants, chloroplasts (photosynthetic plastids) and nuclei change their intracellular positioning in response to light to adapt to fluctuating ambient light conditions, actions known as chloroplast and nuclear photorelocation movement, respectively (2, 3).Although chloroplast photorelocation movement has been studied extensively over the past 100 y (3), nuclear photorelocation movement was analyzed in detail only very recently, in the fern Adiantum capillus-veneris (4). Similar to chloroplasts, nuclei of the fern prothallus are localized to the upper periclinal walls of gametophytic cells under low light conditions (accumulation response) and on anticlinal walls under strong light (avoidance response) (4, 5). Phototropins (phot), which are blue light photoreceptors, and the related photoreceptor neochrome mediate the nuclear and chloroplast movements induced by blue and red light, respectively (6). In the flowering plant Arabidopsis thaliana, ...

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“…The ability to adjust intracellular symbiont position is likely an important means to optimise carbon production, calcification and minimise photosynthetic damage, and can be described as akin to the chloroplastic migration observed in phototrophic organisms, also known as chloroplast photorelocation (Suetsugu and Wada, 2012). This lightdependent process optimises photosynthesis and photoprotection through dispersion or aggregation of the chloroplasts to maximise light capture or shading, respectively (Wada, 2013).…”

Section: Host-mediated Symbiont Photoprotection K Petrou Et Almentioning

confidence: 99%

“…This lightdependent process optimises photosynthesis and photoprotection through dispersion or aggregation of the chloroplasts to maximise light capture or shading, respectively (Wada, 2013). The action of chloroplast photorelocation is driven by the common motor proteins actin and myosin (Suetsugu and Wada, 2012), which together with microtubules are responsible for the movement of cellular organelles in eukaryotic organisms. In the case of photosymbiotic organisms, however, the chloroplast is replaced by an entire algal cell.…”

Section: Host-mediated Symbiont Photoprotection K Petrou Et Almentioning

confidence: 99%

A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera

2016

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Light underpins the health and function of coral reef ecosystems, where symbiotic partnerships with photosynthetic algae constitute the life support system of the reef. Decades of research have given us detailed knowledge of the photoprotective capacity of phototrophic organisms, yet little is known about the role of the host in providing photoprotection in symbiotic systems. Here we show that the intracellular symbionts within the large photosymbiotic foraminifera Marginopora vertebralis exhibit phototactic behaviour, and that the phototactic movement of the symbionts is accomplished by the host, through rapid actin-mediated relocation of the symbionts deeper into the cavities within the calcium carbonate test. Using a photosynthetic inhibitor, we identified that the infochemical signalling for host regulation is photosynthetically derived, highlighting the presence of an intimate communication between the symbiont and the host. Our results emphasise the central importance of the host in photosymbiotic photoprotection via a new mechanism in foraminifera that can serve as a platform for exploring host-symbiont communication in other photosymbiotic organisms.

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Chloroplast Photorelocation Movement: A Sophisticated Strategy for Chloroplasts to Perform Efficient Photosynthesis

Cited by 25 publications

References 63 publications

Phototropin Encoded by a Single-Copy Gene Mediates Chloroplast Photorelocation Movements in the LiverwortMarchantia polymorpha

Phototropin Encoded by a Single-Copy Gene Mediates Chloroplast Photorelocation Movements in the LiverwortMarchantia polymorpha

Actin-dependent plastid movement is required for motive force generation in directional nuclear movement in plants

A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera

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