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EDITORIAL: STATE OF THE FIELD

The Cytoskeleton Becomes Multidisciplinary

Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 (G.O.W.); and Center for Plant Cell Biology, Department of Botany and Plant Sciences, University of California, Riverside, California 92521–0124 (Z.Y.)

It is now becoming clear that the plant cytoskeleton is not just involved in fundamental processes like mitosis, cytokinesis, cell polarity, and intracellular trafficking. For many years, the cortical cytoskeleton's specialized function in plant cell wall construction and morphogenesis has been investigated, but other unique attributes of plants, such as the regulation of water loss through stomatal guard cell movements, pollen tube growth through female reproductive tissue, and elaborations like trichomes and root hairs, also depend on the cytoskeleton. Today it is apparent that the plant cytoskeleton plays an active role in modulating the response of plants to changes in their environment, including encounters with other organisms. It is therefore not surprising that the cytoskeleton is no longer confined to the field of cell biology and that research in a wide range of plant science disciplines, including macromolecular structure, development, hormone action, and environmental stress, will all include important studies on the cytoskeleton. With Plant Physiology's coverage of this wide range of plant science disciplines, a focus issue on the cytoskeleton is timely. Our focus on the cytoskeleton issue begins with four Update articles and includes nine research articles spanning a wide range of disciplines.

It is well established that several hormones including auxins, gibberellins, brassinosteroids, and ethylene influence the organization of cortical actin microfilaments and/or microtubules, implicating a role for these cytoskeletal arrays in hormonal responses. A paper in the November issue of Plant Physiology from Mike Bevan's group (Li et al., 2004) shows that Arabidopsis (Arabidopsis thaliana) mutants, in which a NAP-like gene is knocked out, are affected in sugar responses, implicating actin in the regulation of this process. NAP (NCK-associated protein) is a subunit of the WASP family verprolin homologous protein complex that regulates the conserved actin nucleating Arp2/3 complex. The cytoskeleton has also been implicated in abiotic stress responses such as in osmotic regulation and is known to modulate the activity of ion channels. Both plant-pathogen and symbiotic interactions involve changes in cell polarity and cellular trafficking in plants and thus are intimately associated with the reorganization of the cytoskeleton. An Update article in this issue by Daigo Takemoto and Adrienne Hardham (Takemoto and Hardham, 2004) discusses cytoskeletal responses and functions during encounters between plants and other organisms.

Specific functions of the cytoskeleton depend on how microtubules and microfilaments are distributed and arranged, and how their behavior is modified by proteins that directly associate with both intact polymers and their subunit monomers (Wasteneys and Galway, 2003; Sedbrook, 2004). Significant progress has been made in the identification and functional analysis of cytoskeleton-associated proteins involved in nucleation, membrane anchoring, dynamics (e.g., growing and shrinking of polymers), severing, and polymer cross-linking. In this issue, we highlight the most recent work on the factors influencing microtubule and actin microfilament behavior, and discuss the advantages and limitations of live probes to investigate previously undescribed cytoskeletal functions (Wasteneys and Yang, 2004). Sherryl Bisgrove, Whitney Hable, and Darryl Kropf (Bisgrove et al., 2004) update plus-end tracking proteins, an emerging group of diverse microtubule-associated proteins that may hold the key to understanding how microtubule polarity is put to work in cells. And recent progress in understanding plant motor proteins, including an astounding complement of kinesins and myosins, is covered in an article by Yuh-Ru Lee and Bo Liu (Lee and Liu, 2004).

Two research articles in this issue advance our knowledge of how microtubule-associated proteins (MAPs) work in plant cells. Van Damme et al. (2004; see cover) demonstrate that green fluorescent protein (GFP)-tagged MAP65-1 and MAP65-5 are localized to different subpopulations of cortical microtubules in tobacco BY-2 cells, whereas GFP-MAP65-4 is localized to a specific array of microtubules that rearranged to form spindles. Shoji et al. (2004) identify the SPIRAL2 protein and confirm that this 94-kD HEAT repeat-containing protein interacts with cortical microtubules. Two intriguing findings of this study are that the spr2 mutants have heightened sensitivity to microtubule-disrupting herbicides that target tubulin, and despite the propensity for right-handed twisting in spr2 mutants, when combined with the lefty alpha tubulin point mutations (Thitamadee et al., 2002), left-handed organ twisting is accentuated. The long-recognized biotechnological significance of point mutations in tubulins for effective herbicide use in agriculture is highlighted by Délye and coworkers, who explore the molecular basis for herbicide sensitivity and cross resistance (Délye et al., 2004). It is now clear that microtubule dynamics play an important role in tip-growing root hairs, and in this issue, Van Bruaene et al. (2004) use a MAP4 microtubule binding site-GFP line to follow microtubule organization and behavior. They show for the first time in Arabidopsis root hairs an extensive array of endoplasmic microtubules, and highlight likely search and capture behavior of microtubules in these tip-growing protuberances of root epidermal cells.

On the actin side of the cytoskeleton, a report in this issue by Fan et al. (2004) has identified a novel actin-severing protein from lily, LdABP41, which adds to the growing list of actin-binding proteins mediating actin dynamics and reorganization. The role of the actin cytoskeleton in the modulation of intracellular signaling is highlighted in Wang et al.'s report in this issue describing an inhibitory effect of actin microfilaments on extracellular calcium influxes and cytosolic calcium accumulation in Arabidopsis pollen (Wang et al., 2004).

Developing new ways of documenting the activity and distribution of actin microfilaments remains challenging, and caution is still required in the use of fluorescent fusion proteins. Two articles in this issue focus on the relative advantages and disadvantages of two live probes for labeling actin microfilaments. Ketelaar et al. (2004) demonstrate that GTP-mTalin can alter the dynamic activity of microfilaments, generate defects in cell development, and may not faithfully report all microfilament arrays in plant cells. Similarly, Sheahan et al. (2004) demonstrate how well a GFP construct incorporating one of fimbrin's actin-binding domains works in several plant systems in comparison to available GFP-Talins.

Finally, identifying the functional connections between microtubule and actin microfilament arrays is an area of tremendous importance. An intriguing glimpse is provided in an article published in this issue in which a kinesin with actin microfilament-binding activity and association with cortical arrays in cellulose-rich cotton fibers is identified (Preuss et al., 2004). In future issues of Plant Physiology, we hope to see more studies that consider the functional aspects of actin microfilaments and microtubules as integrated networks in plant cells.

FOOTNOTES

www.plantphysiol.org/cgi/doi/10.1104/pp.104.900130.

^* Corresponding authors; e-mail geoffwas{at}interchange.ubc.ca, zhenbiao.yang{at}ucr.edu; fax 604–822–6089, 951–827–4437.

LITERATURE CITED

Bisgrove SR, Hable WE, Kropf DL (2004) +TIPs and microtubule regulation. The beginning of the plus end in plants. Plant Physiol 136: 3855–3863[Free Full Text]

Délye C, Menchari Y, Michel S, Darmency H (2004) Molecular bases for sensitivity to tubulin-binding herbicides in green foxtail. Plant Physiol 136: 3920–3932[Abstract/Free Full Text]

Fan X, Hou J, Chen X, Chaudhry F, Staiger CJ, Ren H (2004) Identification and characterization of a Ca²⁺-dependent actin filament-severing protein from lily pollen. Plant Physiol 136: 3979–3989[Abstract/Free Full Text]

Ketelaar T, Anthony RG, Hussey PJ (2004) Green fluorescent protein-mTalin causes defects in actin organization and cell expansion in Arabidopsis and inhibits actin depolymerizing factor's actin depolymerizing activity in vitro. Plant Physiol 136: 3990–3998[Abstract/Free Full Text]

Lee Y-RJ, Liu B (2004) Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol 136: 3877–3883[Free Full Text]

Li Y, Sorefan K, Hemmann G, Bevan MW (2004) Arabidopsis NAP and PIR regulate actin-based cell morphogenesis and multiple developmental processes. Plant Physiol 136: 3616–3627[Abstract/Free Full Text]

Preuss ML, Kovar DR, Lee Y-RJ, Staiger CJ, Delmer DP, Liu B (2004) A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol 136: 3945–3955

Sedbrook JC (2004) MAPs in plant cells: delineating microtubule growth dynamics and organization. Curr Opin Plant Biol 7: 632–640[CrossRef][Web of Science][Medline]

Sheahan MB, Staiger CJ, Rose RJ, McCurdy DW (2004) A green fluorescent protein fusion to actin-binding domain 2 of Arabidopsis fimbrin highlights new features of a dynamic actin cytoskeleton in live plant cells. Plant Physiol 136: 3968–3978[Abstract/Free Full Text]

Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T (2004) Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiol 136: 3933–3944[Abstract/Free Full Text]

Takemoto D, Hardham AR (2004) The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136: 3864–3876[Free Full Text]

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Van Bruaene N, Joss G, Van Oostveldt P (2004) Reorganization and in vivo dynamics of microtubules during Arabidopsis root hair development. Plant Physiol 136: 3905–3919[Abstract/Free Full Text]

Van Damme D, Van Poucke K, Boutant E, Ritzenthaler C, Inzé D, Geelen D (2004) In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 136: 3956–3967[Abstract/Free Full Text]

Wang Y-F, Fan L-M, Zhang W-Z, Zhang W, Wu W-H (2004) Ca²⁺-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol 136: 3892–3904[Abstract/Free Full Text]

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