Special Issue: Organelle Motility   

January 2015, Volume 57 Issue 1, Pages 2每135.

Cover Caption: Organelle Motility
About the cover: Actin-dependent chloroplast anchoring is crucial to maintain specific distribution patterns of chloroplasts. Using a centrifugation assay, Sakai et al. (pp. 93每105) demonstrate for the aquatic angiosperm, Vallisneria sp., that an initial step of chloroplast movement in response to high-intensity blue light is loss of anchorage from the plasma membrane. In addition, they clone photoropin 1 & 2, the putatively responsible blue-light photoreceptors, increasing the utility of this experimentally tractable plant for studies of chloroplast motility.


Upward organelle motility  
Author: Tobias I. Baskin
Journal of Integrative Plant Biology 2015 57(1): 2每3
Published Online: December 11, 2014
DOI: 10.1111/jipb.12318
Abstract (Browse 746)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Gustav Senn (1875每1945): The pioneer of chloroplast movement research  
Author: Hironao Kataoka
Journal of Integrative Plant Biology 2015 57(1): 4每13
Published Online: November 18, 2014
DOI: 10.1111/jipb.12311

Gustav Senn analyzed for the first time light-induced movement and arrangement of chloroplasts. Using many plant species he performed physiological analyses of chloroplast migration in response to external stimuli, with emphasis on light. He determined light paths within a cell by measuring refractive indices and optical thickness of cellular compartments and confirmed that chloroplasts migrate towards the region where the light intensity is optimum. After 6 to 7 years' concentrated study, Senn published the famous monograph “Die Gestalts- und Lageveränderung der Pflanzen- Chromatophoren” (The Changes in Shape and Position of Plant Chloroplasts) in 1908. This book has stimulated many plant physiologists and photobiologists, because Senn not only thoroughly classified and defined various types of light-induced chloroplast migration but also already described possible interaction of different photoreceptor systems in Mougeotia more than 50 years before the discovery of phytochrome. This book also contains still useful experimental hints and overlooked findings on the interaction between light and other factors, such as temperature, water content, and nourishment. After publishing this book, Senn retreated from the study of chloroplasts and became a researcher of the Greek philosopher, Theophrastus. In this review, I introduce his biographical background and then summarize some of his key research accomplishment.


Kataoka H (2015) Gustav Senn (1875–1945): The pioneer of chloroplast movement research. J Integr Plant Biol 57: 4–13. doi: 10.1111/jipb.12311

Abstract (Browse 702)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
In 1908 Gustav Senn published a famous book on the photic movement of chloroplasts. He concluded that chloroplasts accumulate in the region where optimally irradiated. Here I provide a brief biography of Gustav Senn and review his achievements, including a diagram explaining the ten types of chloroplast arrangement he documented.
Explaining the ※Pulse of Protoplasm§: The search for molecular mechanisms of protoplasmic streaming  
Author: Michael R. Dietrich
Journal of Integrative Plant Biology 2015 57(1): 14每22
Published Online: December 2, 2014
DOI: 10.1111/jipb.12317

Explanations for protoplasmic streaming began with appeals to contraction in the eighteenth century and ended with appeals to contraction in the twentieth. During the intervening years, biologists proposed a diverse array of mechanisms for streaming motions. This paper focuses on the re-emergence of contraction among the molecular mechanisms proposed for protoplasmic streaming during the twentieth century. The revival of contraction is a result of a broader transition from colloidal chemistry to a macromolecular approach to the chemistry of proteins, the recognition of the phenomena of shuttle streaming and the pulse of protoplasm, and the influential analogy between protoplasmic streaming and muscle contraction.


Dietrich MR (2015) Explaining the“Pulse of Protoplasm”: The search for molecular mechanisms of protoplasmic streaming. J Integr Plant Biol 57: 14–22 doi: 10.1111/jipb.12317

Abstract (Browse 662)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Biologists returned to contraction as a means to explaining motion within the cell in the twentieth century. This preference was a result of the discovery of the pulse motion of protoplasm, the influence of work in muscular contraction, and the transition from colloid chemistry to research on macromolecules.
          Invited Expert Reviews
Role of plant myosins in motile organelles: Is a direct interaction required?  
Author: Limor Buchnik, Mohamad Abu-Abied and Einat Sadot
Journal of Integrative Plant Biology 2015 57(1): 23每30
Published Online: September 5, 2014
DOI: 10.1111/jipb.12282

Plant organelles are highly motile, with speed values of 3–7 µm/s in cells of land plants and about 20–60 µm/s in characean algal cells. This movement is believed to be important for rapid distribution of materials around the cell, for the plant's ability to respond to environmental biotic and abiotic signals and for proper growth. The main machinery that propels motility of organelles within plant cells is based on the actin cytoskeleton and its motor proteins the myosins. Most plants express multiple members of two main classes: myosin VIII and myosin XI. While myosin VIII has been characterized as a slow motor protein, myosins from class XI were found to be the fastest motor proteins known in all kingdoms. Paradoxically, while it was found that myosins from class XI regulate most organelle movement, it is not quite clear how or even if these motor proteins attach to the organelles whose movement they regulate.


Buchnik L, Abu坼Abied M, Sadot E (2015) Role of plant myosins in motile organelles: Is a direct interaction required? J Integr Plant Biol 57: 23–30. doi: 10.1111/jipb.12282

Abstract (Browse 890)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
ROP GTPase-mediated auxin signaling regulates pavement cell interdigitation in Arabidopsis thaliana  
Author: Deshu Lin, Huibo Ren and Ying Fu
Journal of Integrative Plant Biology 2015 57(1): 31每39
Published Online: August 29, 2014
DOI: 10.1111/jipb.12281

In multicellular plant organs, cell shape formation depends on molecular switches to transduce developmental or environmental signals and to coordinate cell-to-cell communication. Plants have a specific subfamily of the Rho GTPase family, usually called Rho of Plants (ROP), which serve as a critical signal transducer involved in many cellular processes. In the last decade, important advances in the ROP-mediated regulation of plant cell morphogenesis have been made by using Arabidopsis thaliana leaf and cotyledon pavement cells. Especially, the auxin-ROP signaling networks have been demonstrated to control interdigitated growth of pavement cells to form jigsaw-puzzle shapes. Here, we review findings related to the discovery of this novel auxin-signaling mechanism at the cell surface. This signaling pathway is to a large extent independent of the well-known Transport Inhibitor Response (TIR)–Auxin Signaling F-Box (AFB) pathway, and instead requires Auxin Binding Protein 1 (ABP1) interaction with the plasma membrane-localized, transmembrane kinase (TMK) receptor-like kinase to regulate ROP proteins. Once activated, ROP influences cytoskeletal organization and inhibits endocytosis of the auxin transporter PIN1. The present review focuses on ROP signaling and its self-organizing feature allowing ROP proteins to serve as a bustling signal decoder and integrator for plant cell morphogenesis.


Lin D, Ren H and Fu Y (2015) ROP GTPase坼mediated auxin signaling regulates pavement cell interdigitation in Arabidopsis thaliana. J Integr Plant Biol 57: 31–39 doi: 10.1111/jipb.12281

Abstract (Browse 1063)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Cell shape formation plays important roles during plant growth and development. Arabidopsis thaliana leaf and cotyledon pavement cells, displaying interdigitated jigsaw-puzzle appearance, provide an ideal model system for studying the mechanism of cell shape formation. Auxin coordinates two Rho GTPase proteins mediated pathways to coordinate the formation of indentations and lobes.
Plant villins: Versatile actin regulatory proteins  
Author: Shanjin Huang, Xiaolu Qu and Ruihui Zhang
Journal of Integrative Plant Biology 2015 57(1): 40每49
Published Online: October 7, 2014
DOI: 10.1111/jipb.12293

Regulation of actin dynamics is a central theme in cell biology that is important for different aspects of cell physiology. Villin, a member of the villin/gelsolin/fragmin superfamily of proteins, is an important regulator of actin. Villins contain six gelsolin homology domains (G1–G6) and an extra headpiece domain. In contrast to their mammalian counterparts, plant villins are expressed widely, implying that plant villins play a more general role in regulating actin dynamics. Some plant villins have a defined role in modifying actin dynamics in the pollen tube; most of their in vivo activities remain to be ascertained. Recently, our understanding of the functions and mechanisms of action for plant villins has progressed rapidly, primarily due to the advent of Arabidopsis thaliana genetic approaches and imaging capabilities that can visualize actin dynamics at the single filament level in vitro and in living plant cells. In this review, we focus on discussing the biochemical activities and modes of regulation of plant villins. Here, we present current understanding of the functions of plant villins. Finally, we highlight some of the key unanswered questions regarding the functions and regulation of plant villins for future research.


Huang S, Qu X, Zhang R (2015) Plant villins: Versatile actin regulatory proteins. J Integr Plant Biol 57: 40–49. doi: 10.1111/jipb.12293

Abstract (Browse 878)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Villin is a versatile actin regulatory protein with actin-nucleating, capping, severing and bundling activity. It is increasingly considered as the major regulator of actin dynamics in plants. In this review article, we summarize our current understanding of plant villins* functions and mechanisms of action.
The endoplasmic reticulum: A dynamic and well-connected organelle  
Author: Chris Hawes, Petra Kiviniemi and Verena Kriechbaumer
Journal of Integrative Plant Biology 2015 57(1): 50每62
Published Online: October 16, 2014
DOI: 10.1111/jipb.12297

The endoplasmic reticulum forms the first compartment in a series of organelles which comprise the secretory pathway. It takes the form of an extremely dynamic and pleomorphic membrane-bounded network of tubules and cisternae which have numerous different cellular functions. In this review, we discuss the nature of endoplasmic reticulum structure and dynamics, its relationship with closely associated organelles, and its possible function as a highway for the distribution and delivery of a diverse range of structures from metabolic complexes to viral particles.


Hawes C, Kiviniemi P, Kriechbaumer V (2015) The endoplasmic reticulum: A dynamic and well-connected organelle. J Integr Plant Biol 57: 50–62. doi: 10.1111/jipb.12297

Abstract (Browse 757)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
In this review we discuss the organisation, dynamics and interactions of an important sub-cellular membrane bounded compartment the endoplasmic reticulum which is responsible for much of the cellular protein processing. We consider the control of its shape, movement, interactions with organelles such as the Golgi, plasma membrane and peroxisomes, plus its role as a surface for metabolic enzymes.
Organelle trafficking, the cytoskeleton, and pollen tube growth  
Author: Giampiero Cai, Luigi Parrotta and Mauro Cresti
Journal of Integrative Plant Biology 2015 57(1): 63每78
Published Online: September 27, 2014
DOI: 10.1111/jipb.12289

The pollen tube is fundamental for the reproduction of seed plants. Characteristically, it grows relatively quickly and uni-directionally (“polarized growth”) to extend the male gametophyte to reach the female gametophyte. The pollen tube forms a channel through which the sperm cells move so that they can reach their targets in the ovule. To grow quickly and directionally, the pollen tube requires an intense movement of organelles and vesicles that allows the cell's contents to be distributed to sustain the growth rate. While the various organelles distribute more or less uniformly within the pollen tube, Golgi-released secretory vesicles accumulate massively at the pollen tube apex, that is, the growing region. This intense movement of organelles and vesicles is dependent on the dynamics of the cytoskeleton, which reorganizes differentially in response to external signals and coordinates membrane trafficking with the growth rate of pollen tubes.


Cai G, Parrotta L, Cresti M (2015) Organelle trafficking, the cytoskeleton, and pollen tube growth. J Integr Plant Biol 57: 63–78. doi: 10.1111/jipb.12289

Abstract (Browse 881)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Organelle movement is essential for the growing plant cells as it allows to deliver specific molecules towards particular cell sites; movement is mostly based on actin filaments and on actin-based motor proteins although microtubules and microtubule-based motor proteins also likely play a subtle but important role.
The pollen tube clear zone: Clues to the mechanism of polarized growth  
Author: Peter K. Hepler and Lawrence J. Winship
Journal of Integrative Plant Biology 2015 57(1): 79每92
Published Online: November 27, 2014
DOI: 10.1111/jipb.12315

Pollen tubes usually exhibit a prominent region at their apex called the “clear zone” because it lacks light refracting amyloplasts. A robust, long clear zone often associates with fast growing pollen tubes, and thus serves as an indicator of pollen tube health. Nevertheless we do not understand how it arises or how it is maintained. Here we review the structure of the clear zone, and attempt to explain the factors that contribute to its formation. While amyloplasts and vacuolar elements are excluded from the clear zone, virtually all other organelles are present including secretory vesicles, mitochondria, Golgi dictyosomes, and the endoplasmic reticulum (ER). Secretory vesicles aggregate into an inverted cone appressed against the apical plasma membrane. ER elements move nearly to the extreme apex, whereas mitochondria and Golgi dictyosomes move less far forward. The cortical actin fringe assumes a central position in the control of clear zone formation and maintenance, given its role in generating cytoplasmic streaming. Other likely factors include the tip-focused calcium gradient, the apical pH gradient, the influx of water, and a host of signaling factors (small G-proteins). We think that the clear zone is an emergent property that depends on the interaction of several factors crucial for polarized growth.


Hepler PK, Winship LJ (2015) The pollen tube clear zone: Clues to the mechanism of polarized growth. J Integr Plant Biol 57: 79–92 doi: 10.1111/jipb.12315

Abstract (Browse 725)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Inside pollen tubes there is continuous lengthwise movement with specific structure. All organelles move tip-wards along the cell boundary, but starch grains and vacuole turn back before reaching the tip, adding to a reverse flow of mitochondria, internal membranes and vesicles back down the center, creating a ※clear zone.§
          Research Articles
Blue-light-induced rapid chloroplast de-anchoring in Vallisneria epidermal cells  
Author: Yuuki Sakai, Shin-ichiro Inoue, Akiko Harada, Ken-ichiro Shimazaki and Shingo Takagi
Journal of Integrative Plant Biology 2015 57(1): 93每105
Published Online: September 17, 2014
DOI: 10.1111/jipb.12284

In the outer periclinal cytoplasm of leaf epidermal cells of an aquatic angiosperm Vallisneria, blue light induces “chloroplast de-anchoring”, a rapid decline in the resistance of chloroplasts against centrifugal force. Chloroplast de-anchoring is known induced within 1 min of irradiation with high-fluence-rate blue light specifically, preceding the commencement of chloroplasts migration toward the anticlinal cytoplasm. However, its regulatory mechanism has remained elusive, although pharmacological analysis suggested that a calcium release from intracellular calcium stores is necessary for the response. In search of the responsible photoreceptors, immunoblotting analysis using antibodies against phototropins demonstrated that cross-reactive polypeptides of 120-kDa exist in the plasma-membrane fraction prepared from the leaves. In vitro phosphorylation analysis revealed that 120-kDa polypeptides were phosphorylated by exposure to blue light in a fluence-dependent manner. The blue-light-induced phosphorylation activity was sensitive to a Ser/Thr kinase inhibitor, staurosporine, and unusually was retained at a high level for a long time in darkness. Furthermore, phototropin gene homologs (Vallisneria PHOTOTROPIN1 and PHOTOTROPIN2) expressed in leaves were isolated. We propose that calcium-regulated chloroplast de-anchoring, possibly mediated by phototropins, is an initial process of the blue-light-induced avoidance response of chloroplasts in Vallisneria.


Sakai Y, Inoue SI, Harada A, Shimazaki KI, Takagi S (2015) Blue坼light坼induced rapid chloroplast de坼anchoring in Vallisneria epidermal cells. J Integr Plant Biol 57: 93–105. doi: 10.1111/jipb.12284

Abstract (Browse 722)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Regulation of intracellular distribution of chloroplasts is important for plants to survive fluctuating environment. A centrifugation method revealed that ※chloroplast de-anchoring§ is an initial process of chloroplast avoidance induced by strong light in an aquatic angiosperm Vallisneria. The response seems to be mediated by blue-light receptor phototropins and cytoplasmic calcium.
The kinesin-like proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens  
Author: Zhiyuan Shen, Yen-Chen Liu, Jeffrey P. Bibeau, Kyle P. Lemoi, Erkan Tüzel and Luis Vidali
Journal of Integrative Plant Biology 2015 57(1): 106每119
Published Online: October 28, 2014
DOI: 10.1111/jipb.12303

In plants, light determines chloroplast position; these organelles show avoidance and accumulation responses in high and low fluence-rate light, respectively. Chloroplast motility in response to light is driven by cytoskeletal elements. The actin cytoskeleton mediates chloroplast photorelocation responses in Arabidopsis thaliana. In contrast, in the moss Physcomitrella patens, both, actin filaments and microtubules can transport chloroplasts. Because of the surprising evidence that two kinesin-like proteins (called KACs) are important for actin-dependent chloroplast photorelocation in vascular plants, we wanted to determine the cytoskeletal system responsible for the function of these proteins in moss. We performed gene-specific silencing using RNA interference in P. patens. We confirmed existing reports using gene knockouts, that PpKAC1 and PpKAC2 are required for chloroplast dispersion under uniform white light conditions, and that the two proteins are functionally equivalent. To address the specific cytoskeletal elements responsible for motility, this loss-of-function approach was combined with cytoskeleton-targeted drug studies. We found that, in P. patens, these KACs mediate the chloroplast light-avoidance response in an actin filament-dependent, rather than a microtubule-dependent manner. Using correlation-decay analysis of cytoskeletal dynamics, we found that PpKAC stabilizes cortical actin filaments, but has no effect on microtubule dynamics.


Shen Z, Liu YC, Bibeau JP, Lemoi KP, Tüzel E, Vidali L (2015) The kinesin-like proteins, KAC1/2, regulate actin dynamics underlying chloroplast light-avoidance in Physcomitrella patens. J Integr Plant Biol 57: 106–119. doi: 10.1111/jipb.12303

Abstract (Browse 726)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Chloroplast movements in response to light are important for plant adaptation to light conditions. This work shows that in moss, the function of the kinesin-related protein, PpKAC, is important for actin but not microtubule-dependent light avoidance. It also shows that PpKAC may participate in this process by stabilizing actin filaments.
Clues to the signals for chloroplast photo-relocation from the lifetimes of accumulation and avoidance responses  
Author: Takeshi Higa and Masamitsu Wada
Journal of Integrative Plant Biology 2015 57(1): 120每126
Published Online: November 5, 2014
DOI: 10.1111/jipb.12310

Chloroplast photo-relocation movement is crucial for plant survival; however, the mechanism of this phenomenon is still poorly understood. Especially, the signal that goes from photoreceptor to chloroplast is unknown, although the photoreceptors (phototropin 1 and 2) have been identified and an actin structure (chloroplast actin filaments) has been characterized that is specific for chloroplast movement. Here, in gametophytes of the fern Adiantum capillus-veneris, gametophores of the moss Physcomiterella patens, and leaves of the seed plant Arabidopsis thaliana, we sought to characterize the signaling system by measuring the lifetime of the induced response. Chloroplast movements were induced by microbeam irradiation with high-intensity blue light and recorded. The lifetime of the avoidance state was measured as a lag time between switching off the beam and the loss of avoidance behavior, and that of the accumulation state was measured as the duration of accumulation behavior following the extinction of the beam. The lifetime for the avoidance response state is approximately 3–4 min and that for the accumulation response is 19–28 min. These data suggest that the two responses are based on distinct signals.


Higa T and Wada M (2015) Clues to the signals for chloroplast photo-relocation from the lifetimes of accumulation and avoidance responses. J Integr Plant Biol 57: 120–126. doi: 10.1111/jipb.12310

Abstract (Browse 705)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Signal(s) transferred from photoreceptors (phototropins) to chloroplasts in chloroplast photorelocation movement is still unknown. The durations of chloroplast avoidance and following accumulation response after partial cell irradiation with strong blue light were quite different, suggesting that the signals and the signal lifetimes of the two responses are different each other.
Simplification of vacuole structure during plant cell death triggered by culture filtrates of Erwinia carotovora  
Author: Yumi Hirakawa, Toshihisa Nomura, Seiichiro Hasezawa and Takumi Higaki
Journal of Integrative Plant Biology 2015 57(1): 127每135
Published Online: October 31, 2014
DOI: 10.1111/jipb.12304

Vacuoles are suggested to play crucial roles in plant defense-related cell death. During programmed cell death, previous live cell imaging studies have observed vacuoles to become simpler in structure and have implicated this simplification as a prelude to the vacuole's rupture and consequent lysis of the plasma membrane. Here, we examined dynamics of the vacuole in cell cycle-synchronized tobacco BY-2 (Nicotiana tabacum L. cv. Bright Yellow 2) cells during cell death induced by application of culture filtrates of Erwinia carotovora. The filtrate induced death in about 90% of the cells by 24 h. Prior to cell death, vacuole shape simplified and endoplasmic actin filaments disassembled; however, the vacuoles did not rupture until after plasma membrane integrity was lost. Instead of facilitating rupture, the simplification of vacuole structure might play a role in the retrieval of membrane components needed for defense-related cell death.


Hirakawa Y, Nomura T, Hasezawa S, Higaki T (2015) Simplification of vacuole structure during plant cell death triggered by culturefiltrates of Erwinia carotovora. J Integr Plant Biol 57: 127–135. doi: 10.1111/jipb.12304

Abstract (Browse 753)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
In defense-related cell death, vacuole simplification has been considered as a prelude to the vacuole*s rupture. Hirakawa et al. discovered a new type of the cell death that vacuoles become simpler but maintain their integrity at the onset of cell death. The results call for rethinking the roles of vacuole simplification.
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