JIPB
Journal of Integrative Plant Biology
Free Access
Editorial
Upward organelle motility Eukaryotic cells contain a collection of membrane-bounded organelles, in addition to the nucleus, supporting the large size and diverse activities of this type of cell. Evolving with these compartments are filaments and enzymes that convert chemical energy into work (so-called motor proteins), a network collectively termed the cytoskeleton. Whether it is a chloroplast moving to optimally intercept light or the endoplasmic reticulum deploying its cisternae to deliver secreted proteins, motility of organelles is an essential component of their function, and this motility is driven by the cytoskeleton. Recent research on organelle movement, revealing cytoskeletal and organelle function, is surveyed here in this special issue of Journal of Integrative Plant Biology (JIPB). The issue contains twelve articles, divided more or less equally between reviews and primary research. Although authors were invited based on their past accomplishments, all papers were subject to JIPB’s rigorous peer review. Here I provide brief summaries of the papers and conclude with a comment about the cytoskeleton and motility. Unusual perhaps for a science journal, the first two papers are historical. In 1908, Gustav Senn published a monograph in German on chloroplast motility, an exhaustive study that inaugurated modern understanding of this process. Kataoka (2015) provides a concise summary, which is not only intrinsically interesting but will repay interest from a modern scientist looking for useful experimental material or valuable ideas. Dr. Kataoka recently translated Senn’s book into Japanese and I hope that readers will be motivated to produce English and Chinese versions. The second article, by Dr. Dietrich (2015), a historian of biology at Dartmouth, is an investigation into how cytoplasmic streaming has been understood, starting from the mysterious colloids of the nineteenth century and reaching all the way to the acto-myosin of today. Interviewing participants and consulting correspondence between principals, Dietrich tells a fascinating story. Moreover, as the review on myosin in this issue argues (Buchnik et al. 2015), the familiar picture of a myosin motor walking down an actin track might be insufficient to explain all aspects of streaming and some of these early ideas might need resurrection. Beside the review on myosin just mentioned, the issue contains reviews on two other protein families. Lin et al. (2015) review the small G-proteins known as Rho of plants (ROP), focusing specifically on the role of these essential signaling molecules in the formation of cell lobes by leaf epidermal cells in Arabidopsis thaliana. Among other things, the review brings readers up to date on lobe formation, a process where the cytoskeleton and motility are being productively explored. Research on G-proteins is challenging because they breed in teeming families and even wild-type versions can gain functions when expressed too highly, challenges that need to be kept in mind when evaluating research on these pivotal molecules. The other protein-centric review (Huang et al. 2015) concerns villins, a versatile group of actin-binding proteins named from their early discovered role in forming the protuberances of intestinal microvilli. In plants, no unmistakably “villainous” structure exists but there has been a sizable January 2015 | Volume 57 | Issue 1 | 2–3
collection of studies by now elucidating structures and functions of plant villins and this review provides a timely overview. The remaining three reviews are up a few levels of scale from the single protein level. Hawes et al. (2015) survey the endoplasmic reticulum. While the role of this organelle in synthesizing secreted proteins is familiar, less well known is its role in other functions, such as forming a platform for organizing metabolic pathways. Hawes et al. present a conspectus of ER function, treating as expected the complex motility of this organelle, with its myriad tubules and cisternae, but also treating diverse activities of this central organelle. Given the pervasiveness of the ER throughout the cell, it is not surprising that it extends a tubule into many cellular pies, so much so that despite the comprehensiveness of Hawes et al.’s treatment, readers might yet find something omitted. The final two reviews concern the pollen tube. Cai et al. (2015) provide a sweeping account of the major organelles and how they move while Hepler and Winship (2015) concentrate on the clear zone at the tip of the pollen tube, which they describe as enigmatic. That there is a relatively organelle-free zone at the tip of the pollen tube despite the vigorous cytoplasmic streaming defies ready explanation, even though motility and the cytoskeleton have been extensively studied in pollen tubes, as the large number of references cited by Cai et al. will attest. Hepler and Winship discuss the idea that the clear zone might arise from highly localized water influx. Hydraulics are often neglected because water is everywhere and these authors’ proposal is sure to inspire comment and further research. Turning to research articles, three of the four concern chloroplast motility in response to light. This dominance is perhaps not surprising given the importance of photosynthesis and the relative ease of imaging chloroplasts. Attention to mechanisms for moving them makes sense. Sakai et al. (2015) study how chloroplasts avoid bright light (the so-called avoidance response) in the leaves of an aquatic angiosperm (a species of Vallisneria). They clone the putatively responsible photoreceptors, phototropin1 and 2, and elucidate a pathway in which phototropin activation by bright light causes the chloroplasts to lose anchorage and then be subject to the motility machinery for relocation. This constitutes a notable advance in our understanding of the mechanisms of chloroplast avoidance responses. Like that of nearly all plant organelles, chloroplast motility is controlled by the actin cytoskeleton. It was thus a puzzle when, a few years ago, two proteins involved in chloroplast photo-relocation were found to be kinesins, proteins defined by their activity against microtubules. Shen et al. (2015) exploit the powerful moss, Physcomitrella patens, to support the idea that the two kinesins act via actin rather than microtubules. Although there are caveats, their principal findings are that the double loss-of-function mutant has residual light-dependent chloroplast motility that is insensitive to actin inhibitors but responsive to microtubule inhibitors and that this mutant has altered cytoskeletal dynamics for actin but not for microtubules. This appears to be a striking example of the www.jipb.net
Editorial promiscuity of evolution where a seemingly respectable kinesin abandons its microtubules to hook up with a new partner; I look forward to learning about the molecular details of this affair. The third article on chloroplast photo-relocation is perhaps the subtlest. Higa and Wada (2015) recognize a crater-sized gap in our understanding: we have identified and characterized the relevant photoreceptors; we have a reasonable understanding of how the actin cytoskeleton ferries the chloroplasts around the cell in the presence of light stimuli; but how are these linked? Higa and Wada conceptualize this as a signal moving between photoreceptor and chloroplast, although in principle the linkage could be far more complex than a small, diffusing molecule. These authors do elegant experiments to measure how long the signal (thus defined) persists and show that the signal for avoidance is fleeting (3 min) compared to that for accumulation (24 min). Although just a shovelful, this begins to fill in the aforementioned crater. The final paper is arguably the most curious – it concerns the reorganization of the vacuole as a cell undergoes programmed cell death. The central vacuole of large plant cells tends to be visualized as a sac filled with toxic secondary metabolites, the bane of herbivores and biochemists. But these vacuoles often have ornate shapes and undergo profound morphological rearrangement, as for example when a cell is stimulated to divide. Similarly, when a large cell is induced to die, the vacuole often simplifies its shape. Hirakawa et al. (2015) using BY-2 cells induced to die by exposure to filtrates from pathogen culture, falsify the hypothesis that the simplification serves as a prelude to vacuole rupture and actual cell death. In fact, the cell dies before the vacuole ruptures, leaving the reason for vacuole simplification as an exercise for further research. To the uninitiated, the word cytoskeleton might conjure up images of microscopic bones, an armature upon which the parts of a cell can rest. But plant cells receive plenty of support from their cell walls and few plant scientists visualize the cytoskeleton as femur, pelvis, and rib. Instead, recognizing that cytoskeletal filaments pervade the cell, we visualize the cytoskeleton as a transportation system, moving material throughout the cell. Indeed, we call this flow traffic, and routinely describe cytoskeletal activity with words like track and motor. Even so, thinking of the cytoskeleton as trains on tracks misses an essential attribute. The cytoskeleton is dynamic, with its filaments turning over on a time scale commensurate with the very traffic flows being supported, rather as if one were to drive down a highway with bulldozers in front and jackhammers behind. Cytoskeletal dynamics are local, distributed, and flexible. Fluctuations in cytoskeletal structure can propagate faster than diffusion and thus allow the whole cell to be informed and to respond. In this respect, the cytoskeleton seems oddly like social media. A cell-phone network allows thousands of humans to behave coherently even though no
www.jipb.net
3
one person is in charge. Thinking of the cytoskeleton as cytomedia is perhaps fanciful, but it does emphasize the oftenneglected, informational role of the cell’s bones. Not all signal transduction cascades lead to the nucleus, many ramify through the cytoplasm. Organelle motility provides a conspicuous readout of this cellular “paracrine” system and as a consequence represents a fruitful mode for discovering the mechanisms of cellular animation. Tobias I. Baskin, Professor Special Issue Editor Centre for Plant Integrative Biology, University of Nottingham, UK & Biology Department, University of Massachusetts Amherst, MA, USA doi: 10.1111/jipb.12318 © 2014 Institute of Botany, Chinese Academy of Sciences
REFERENCES Buchnik L, Abu-Abied M, Sadot E (2015) Role of plant myosins in motile organelles: Is a direct interaction required? J Integr Plant Biol 57: 23–30 Cai G, Parrotta L, Cresti M (2015) Organelle trafficking, the cytoskeleton, and pollen tube growth. J Integr Plant Biol 57: 63–78 Dietrich M (2015) Explaining the “pulse of protoplasm”: The search for molecular mechanisms of protoplasmic streaming. J Integr Plant Biol 57: 14–22 Hawes C, Kiviniemi P, Kriechbaumer V (2015) The endoplasmic reticulum: A dynamic and well connected organelle. J Integr Plant Biol 57: 50–62 Hepler PK, Winship L (2015) The pollen tube clear zone: Clues to the mechanism of polarized growth. J Integr Plant Biol 57: 79–92 Higa T, Wada M (2015) Clues to the signals for chloroplast photorelocation from the lifetimes of accumulation and avoidance responses. J Integr Plant Biol 57: 120–126 Hirakawa Y, Nomura T, Hasezawa S, Higaki T (2015) Simplification of vacuole structure during plant cell death triggered by culture filtrates of Erwinia carotovora. J Integr Plant Biol 57: 127–135 Huang S, Qu X, Zhang R (2015) Plant villins: Versatile actin regulatory proteins. J Integr Plant Biol 57: 40–49 Kataoka H (2015) Gustav Senn (1875–1945): The pioneer of chloroplast movement research. J Integr Plant Biol 57: 4–13 Lin D, Ren H, Fu Y (2015) ROP GTPase-mediated auxin signaling regulates pavement cell interdigitation in Arabidopsis thaliana. J Integr Plant Biol 57: 31–39 Sakai Y, Inoue SI, Harada A, Shimazaki KI, Takagi S (2015) Blue-lightinduced rapid chloroplast de-anchoring in Vallisneria epidermal cells. J Integr Plant Biol 57: 93–105 Shen Z, Liu YC, Bibeau JP, Lemoi KP, Tüzel E, Vidali L (2015) The kinesinlike proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens. J Integr Plant Biol 57: 106–119
January 2015 | Volume 57 | Issue 1 | 2–3
Journal of Integrative Plant Biology
Free Access
Editorial
Upward organelle motility Eukaryotic cells contain a collection of membrane-bounded organelles, in addition to the nucleus, supporting the large size and diverse activities of this type of cell. Evolving with these compartments are filaments and enzymes that convert chemical energy into work (so-called motor proteins), a network collectively termed the cytoskeleton. Whether it is a chloroplast moving to optimally intercept light or the endoplasmic reticulum deploying its cisternae to deliver secreted proteins, motility of organelles is an essential component of their function, and this motility is driven by the cytoskeleton. Recent research on organelle movement, revealing cytoskeletal and organelle function, is surveyed here in this special issue of Journal of Integrative Plant Biology (JIPB). The issue contains twelve articles, divided more or less equally between reviews and primary research. Although authors were invited based on their past accomplishments, all papers were subject to JIPB’s rigorous peer review. Here I provide brief summaries of the papers and conclude with a comment about the cytoskeleton and motility. Unusual perhaps for a science journal, the first two papers are historical. In 1908, Gustav Senn published a monograph in German on chloroplast motility, an exhaustive study that inaugurated modern understanding of this process. Kataoka (2015) provides a concise summary, which is not only intrinsically interesting but will repay interest from a modern scientist looking for useful experimental material or valuable ideas. Dr. Kataoka recently translated Senn’s book into Japanese and I hope that readers will be motivated to produce English and Chinese versions. The second article, by Dr. Dietrich (2015), a historian of biology at Dartmouth, is an investigation into how cytoplasmic streaming has been understood, starting from the mysterious colloids of the nineteenth century and reaching all the way to the acto-myosin of today. Interviewing participants and consulting correspondence between principals, Dietrich tells a fascinating story. Moreover, as the review on myosin in this issue argues (Buchnik et al. 2015), the familiar picture of a myosin motor walking down an actin track might be insufficient to explain all aspects of streaming and some of these early ideas might need resurrection. Beside the review on myosin just mentioned, the issue contains reviews on two other protein families. Lin et al. (2015) review the small G-proteins known as Rho of plants (ROP), focusing specifically on the role of these essential signaling molecules in the formation of cell lobes by leaf epidermal cells in Arabidopsis thaliana. Among other things, the review brings readers up to date on lobe formation, a process where the cytoskeleton and motility are being productively explored. Research on G-proteins is challenging because they breed in teeming families and even wild-type versions can gain functions when expressed too highly, challenges that need to be kept in mind when evaluating research on these pivotal molecules. The other protein-centric review (Huang et al. 2015) concerns villins, a versatile group of actin-binding proteins named from their early discovered role in forming the protuberances of intestinal microvilli. In plants, no unmistakably “villainous” structure exists but there has been a sizable January 2015 | Volume 57 | Issue 1 | 2–3
collection of studies by now elucidating structures and functions of plant villins and this review provides a timely overview. The remaining three reviews are up a few levels of scale from the single protein level. Hawes et al. (2015) survey the endoplasmic reticulum. While the role of this organelle in synthesizing secreted proteins is familiar, less well known is its role in other functions, such as forming a platform for organizing metabolic pathways. Hawes et al. present a conspectus of ER function, treating as expected the complex motility of this organelle, with its myriad tubules and cisternae, but also treating diverse activities of this central organelle. Given the pervasiveness of the ER throughout the cell, it is not surprising that it extends a tubule into many cellular pies, so much so that despite the comprehensiveness of Hawes et al.’s treatment, readers might yet find something omitted. The final two reviews concern the pollen tube. Cai et al. (2015) provide a sweeping account of the major organelles and how they move while Hepler and Winship (2015) concentrate on the clear zone at the tip of the pollen tube, which they describe as enigmatic. That there is a relatively organelle-free zone at the tip of the pollen tube despite the vigorous cytoplasmic streaming defies ready explanation, even though motility and the cytoskeleton have been extensively studied in pollen tubes, as the large number of references cited by Cai et al. will attest. Hepler and Winship discuss the idea that the clear zone might arise from highly localized water influx. Hydraulics are often neglected because water is everywhere and these authors’ proposal is sure to inspire comment and further research. Turning to research articles, three of the four concern chloroplast motility in response to light. This dominance is perhaps not surprising given the importance of photosynthesis and the relative ease of imaging chloroplasts. Attention to mechanisms for moving them makes sense. Sakai et al. (2015) study how chloroplasts avoid bright light (the so-called avoidance response) in the leaves of an aquatic angiosperm (a species of Vallisneria). They clone the putatively responsible photoreceptors, phototropin1 and 2, and elucidate a pathway in which phototropin activation by bright light causes the chloroplasts to lose anchorage and then be subject to the motility machinery for relocation. This constitutes a notable advance in our understanding of the mechanisms of chloroplast avoidance responses. Like that of nearly all plant organelles, chloroplast motility is controlled by the actin cytoskeleton. It was thus a puzzle when, a few years ago, two proteins involved in chloroplast photo-relocation were found to be kinesins, proteins defined by their activity against microtubules. Shen et al. (2015) exploit the powerful moss, Physcomitrella patens, to support the idea that the two kinesins act via actin rather than microtubules. Although there are caveats, their principal findings are that the double loss-of-function mutant has residual light-dependent chloroplast motility that is insensitive to actin inhibitors but responsive to microtubule inhibitors and that this mutant has altered cytoskeletal dynamics for actin but not for microtubules. This appears to be a striking example of the www.jipb.net
Editorial promiscuity of evolution where a seemingly respectable kinesin abandons its microtubules to hook up with a new partner; I look forward to learning about the molecular details of this affair. The third article on chloroplast photo-relocation is perhaps the subtlest. Higa and Wada (2015) recognize a crater-sized gap in our understanding: we have identified and characterized the relevant photoreceptors; we have a reasonable understanding of how the actin cytoskeleton ferries the chloroplasts around the cell in the presence of light stimuli; but how are these linked? Higa and Wada conceptualize this as a signal moving between photoreceptor and chloroplast, although in principle the linkage could be far more complex than a small, diffusing molecule. These authors do elegant experiments to measure how long the signal (thus defined) persists and show that the signal for avoidance is fleeting (3 min) compared to that for accumulation (24 min). Although just a shovelful, this begins to fill in the aforementioned crater. The final paper is arguably the most curious – it concerns the reorganization of the vacuole as a cell undergoes programmed cell death. The central vacuole of large plant cells tends to be visualized as a sac filled with toxic secondary metabolites, the bane of herbivores and biochemists. But these vacuoles often have ornate shapes and undergo profound morphological rearrangement, as for example when a cell is stimulated to divide. Similarly, when a large cell is induced to die, the vacuole often simplifies its shape. Hirakawa et al. (2015) using BY-2 cells induced to die by exposure to filtrates from pathogen culture, falsify the hypothesis that the simplification serves as a prelude to vacuole rupture and actual cell death. In fact, the cell dies before the vacuole ruptures, leaving the reason for vacuole simplification as an exercise for further research. To the uninitiated, the word cytoskeleton might conjure up images of microscopic bones, an armature upon which the parts of a cell can rest. But plant cells receive plenty of support from their cell walls and few plant scientists visualize the cytoskeleton as femur, pelvis, and rib. Instead, recognizing that cytoskeletal filaments pervade the cell, we visualize the cytoskeleton as a transportation system, moving material throughout the cell. Indeed, we call this flow traffic, and routinely describe cytoskeletal activity with words like track and motor. Even so, thinking of the cytoskeleton as trains on tracks misses an essential attribute. The cytoskeleton is dynamic, with its filaments turning over on a time scale commensurate with the very traffic flows being supported, rather as if one were to drive down a highway with bulldozers in front and jackhammers behind. Cytoskeletal dynamics are local, distributed, and flexible. Fluctuations in cytoskeletal structure can propagate faster than diffusion and thus allow the whole cell to be informed and to respond. In this respect, the cytoskeleton seems oddly like social media. A cell-phone network allows thousands of humans to behave coherently even though no
www.jipb.net
3
one person is in charge. Thinking of the cytoskeleton as cytomedia is perhaps fanciful, but it does emphasize the oftenneglected, informational role of the cell’s bones. Not all signal transduction cascades lead to the nucleus, many ramify through the cytoplasm. Organelle motility provides a conspicuous readout of this cellular “paracrine” system and as a consequence represents a fruitful mode for discovering the mechanisms of cellular animation. Tobias I. Baskin, Professor Special Issue Editor Centre for Plant Integrative Biology, University of Nottingham, UK & Biology Department, University of Massachusetts Amherst, MA, USA doi: 10.1111/jipb.12318 © 2014 Institute of Botany, Chinese Academy of Sciences
REFERENCES Buchnik L, Abu-Abied M, Sadot E (2015) Role of plant myosins in motile organelles: Is a direct interaction required? J Integr Plant Biol 57: 23–30 Cai G, Parrotta L, Cresti M (2015) Organelle trafficking, the cytoskeleton, and pollen tube growth. J Integr Plant Biol 57: 63–78 Dietrich M (2015) Explaining the “pulse of protoplasm”: The search for molecular mechanisms of protoplasmic streaming. J Integr Plant Biol 57: 14–22 Hawes C, Kiviniemi P, Kriechbaumer V (2015) The endoplasmic reticulum: A dynamic and well connected organelle. J Integr Plant Biol 57: 50–62 Hepler PK, Winship L (2015) The pollen tube clear zone: Clues to the mechanism of polarized growth. J Integr Plant Biol 57: 79–92 Higa T, Wada M (2015) Clues to the signals for chloroplast photorelocation from the lifetimes of accumulation and avoidance responses. J Integr Plant Biol 57: 120–126 Hirakawa Y, Nomura T, Hasezawa S, Higaki T (2015) Simplification of vacuole structure during plant cell death triggered by culture filtrates of Erwinia carotovora. J Integr Plant Biol 57: 127–135 Huang S, Qu X, Zhang R (2015) Plant villins: Versatile actin regulatory proteins. J Integr Plant Biol 57: 40–49 Kataoka H (2015) Gustav Senn (1875–1945): The pioneer of chloroplast movement research. J Integr Plant Biol 57: 4–13 Lin D, Ren H, Fu Y (2015) ROP GTPase-mediated auxin signaling regulates pavement cell interdigitation in Arabidopsis thaliana. J Integr Plant Biol 57: 31–39 Sakai Y, Inoue SI, Harada A, Shimazaki KI, Takagi S (2015) Blue-lightinduced rapid chloroplast de-anchoring in Vallisneria epidermal cells. J Integr Plant Biol 57: 93–105 Shen Z, Liu YC, Bibeau JP, Lemoi KP, Tüzel E, Vidali L (2015) The kinesinlike proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens. J Integr Plant Biol 57: 106–119
January 2015 | Volume 57 | Issue 1 | 2–3
