JXB Advance Access originally published online on April 2, 2007
Journal of Experimental Botany 2007 58(7):1843-1849; doi:10.1093/jxb/erm047
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens
Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, UK
* To whom correspondence should be addressed. E-mail: liam.dolan{at}bbsrc.ac.uk
Received 16 November 2006; Revised 29 January 2007 Accepted 21 February 2007
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Abstract |
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Tip growth is a mode of cell expansion in which all growth is restricted to a small area that forms a tip in an elongating cell. In green plants, tip growth has been shown to occur in root hairs, pollen tubes, rhizoids, and caulonema. Each of these cell types has a longitudinally elongated shape, longitudinally oriented microtubules and actin microfilaments, and a characteristic cytoplasmic organization at the growing tip which is required for growth. Chloronema are elongated cylindrical shaped cells that form during the development of the moss protonema. Since there are no published reports on the precise mode of chloronema elongation and conflicting interpretations of its cytology, the mechanism of cell growth has remained unclear. To determine if chloronema elongate by tip or diffuse growth, time-lapse light microscopy was employed to follow the movement of fluorescent microspheres attached to the surface of growing cells. It is shown here that chloronemal cells elongate by a form of tip growth. However, the slower growth of chloronema compared with caulonema is probably the result of differences in cytological organization of the growing tip.
Key words: Caulonema, chloronema, diffuse growth, fluorescent beads, Physcomitrella patens, time-lapse, tip growth
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Introduction |
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Over the past 450 million years land plant bodies have radically changed with the invention of new cell and tissue systems (Davis and Kenrick, 2004). Plant cells have evolved a variety of shapes with diverse morphologies and specialized functions. Most plant cells grow by diffuse (intercalary) growth in which expansion of the cell wall is distributed over large areas of the cell surface (Smith, 2003). However, some cells grow by a highly polarized mechanism in which cell wall extension is restricted to a localized region at the tip of the cell (Carol and Dolan, 2002; Smith, 2003). This mode of cell expansion is called tip growth and has been well characterized in root hairs, pollen tubes, and rhizoids of many plants. Root hairs are root epidermal cell outgrowths that increase the surface of the root in contact with the soil. The pollen tube develops during germination of the pollen grain and delivers the male gamete nuclei to the ovule. Root hairs and pollen tubes have longitudinally oriented actin bundles and microtubules, and have a clear region of cytoplasm and vesicle accumulation at their tip, called the tip body (Carol and Dolan, 2002; Smith, 2003). A tip high calcium gradient is established through a molecular mechanism involving small GTPases (Foreman et al., 2003; Carol et al., 2005; Gu et al., 2005). Rhizoids are multicellular or unicellular cylindrical cells that develop in many groups of land plants and in green algae such as Chara vulgaris (Braun, 1997; Braun et al., 2004). Tip growth has also been described in organisms not related to green plants such as brown algae (Heterokonts) and filamentous fungi, indicating that this process evolved many times independently during the evolution of the eukaryotes (Horio and Oakley, 2005; Katsaros et al., 2006). The extreme morphological polarity of cells does not necessarily imply that they elongate by tip growth. For example, unbranched trichomes such as cotton fibres have been shown to grow by diffuse growth despite being highly polarized (Tiwari and Wilkins, 1995). Therefore, an elongated shape and a high cell polarity are not sufficient criteria to determine that a cell is growing by tip growth.
The filamentous protonema stage of the gametophyte of mosses has a relatively simple organization and can be grown easily in vitro (Cove, 2005). The moss protonema comprises two cell types with elongated shape: the chloronema and the caulonema (Fig. 1). Chloronemal cells contain many large chloroplasts and are principally involved in photosynthesis, whereas the main roles of the caulonemal cells, which contain fewer plastids, are substrate colonization and nutrient acquisition. The protonema develops immediately after spore germination and at first it consists entirely of chloronema. Depending on the species and the environment, the protonema may remain chloronemal or it may develop as a colony comprising both chloronema and caulonema. The individual cells of the caulonema are longer and narrower than chloronemal cells. It has been demonstrated that caulonema cells contain a longitudinal array of microtubules, a clear tip body, have a tip high calcium gradient, and grow at a similar rate to root hairs (20–30 µm h–1) (Reiss and Herth, 1979; Schmiedel and Schnepf, 1980; Doonan et al., 1985). Together these data indicate that caulonema are tip growing and that their growth mechanism resembles that of other tip-growing cells such as pollen tubes and root hairs. While it is often assumed that chloronemal cells elongate by tip growth, there has been no demonstration that tip growth operates in these cells (Doonan et al., 1985; Duckett et al., 1998; Harries et al., 2005). Although there is some indirect evidence that is consistent with their elongation by tip growth, such as the tip accumulation of arabinogalactan proteins that are involved in growth (Lee et al., 2005), there is other evidence that suggests that these cells cannot elongate by typical tip growth. Such evidence includes their slow growth rate (4–10 µm h–1), the presence of dividing chloroplasts within the apical dome, the absence of a distinct tip-growing cytological organization at the end of a cell where growth would be expected to occur, and the absence of DiOC6 staining at the tip (DiOC6 is a fluorochrome that stains organelles preferentially in cells with a high level of exocytotic activity) (Duckett et al., 1998). Together these data call into question the ‘assumed’ mechanism of tip growth of these cells and have led to a suggestion that chloronemal cells may in fact elongate by diffuse (intercalary) growth (Duckett et al., 1998). Therefore, to understand the developmental mechanism underpinning the development of the moss gametophyte, it is necessary to determine if chloronemal cells grow by tip growth or if, like the polar cotton fibre, they expand by diffuse growth.
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Here, the mode of growth found in chloronemal and caulonemal cells of Physcomitrella patens was determined using time-lapse microscopy to follow the movement of fluorescent microspheres attached to the surface of growing cells. This method, which has been used previously with Medicago truncatula root hairs (Shaw et al., 2000), allowed discrimination between diffuse growth and tip growth in growing chloronema.
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Materials and methods |
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Material and growth conditions
Nicotiana tabacum BY-2 (Bright yellow) cells were grown in the dark at 25 °C with 150 rpm agitation in liquid BY-2 medium (Nagata et al., 1992).
The Gransden wild-type strain of P. patens (Hedw.) Br. Eur. [Aphanorhegma patens (Hedw.) Lindb] was used in this study (Ashton and Cove, 1977). Cultures were grown at 25 °C and illuminated with a light regime of 16/8 h light/dark and a quantum irradiance of 40 µE m–2 s–1. Protonema enriched in chloronemal cells were obtained by culture on solid (1% agar) minimal medium supplemented with 0.5% sucrose and 5 mM ammonium tartrate, whereas minimal medium was used for caulonemal cells (Ashton et al., 1979).
Time-lapse experiments
The fluorescent microspheres used are the FluoSpheres sulphate microspheres, 0.2 µm, yellow-green fluorescent (reference F8848, Invitrogen, Carlsbad, CA, USA). The microspheres were washed five times in water before use. Six-day-old protonema or BY-2 cell cultures were incubated for 5 min in 0.02% microspheres in the appropriate liquid medium, washed in liquid medium, and rapidly placed in a chamber fitted with a gas-permeable membrane (bioFOLIE; VivaScience, Goettingen, Germany) (Chan et al., 2005). Caulonema- and chloronema-enriched cell cultures were continuously illuminated with a quantum irradiance of 5 mE m–2 s–1 and 40 mE m–2 s–1, respectively. Cells labelled through all their surface were chosen for time-lapse experiments.
Microscopy data acquisition and analysis
Images were acquired on a Nikon Eclipse 600 microscope (Nikon UK Ltd, Kingston upon Thames, UK) equipped with a Hamamatsu Orca AG cooled CCD camera (Hamamatsu Photonics UK Ltd, Welwyn Garden City, Hertfordshire, UK) using an x20/0.5 objective. The fluorescent microspheres were excited using 480–500 nm light from a mercury arc lamp and visualized at 509–547 nm. The time interval between each data acquisition period was 1 h for BY-2 cells and 30 min for chloronemal and caulonemal cells. A z-axial series with steps of 3 µm was collected for each time interval, and maximum projection images were generated using either Metamorph (Molecular Devices Corporation, Dowingtown, PA, USA) or ImageJ (http://rsb.info.nih.gov/ij/) software.
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Results |
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Setting up experimental conditions to distinguish between tip growth and diffuse growth
Sulphated microspheres were used to mark the cell surface of growing cells. They have previously been shown to adhere to the surface of a plant cell without perturbing cell growth (Shaw et al., 2000). To label the entire cell surface, the cells were briefly incubated in a microsphere solution just before the time-lapse experiment was initiated. Two kinds of growth rate have been measured. The mean growth rate of a cell (Table 1) is the mean rate of extension of all the cells analysed. It was obtained by measuring the length of each cell (from cross wall to cross wall or from cross wall to tip) at two time intervals. The growth rate between two microspheres (Table 2) reflects local growth rate. It was obtained by measuring the distance between two microspheres at two time intervals. Thus it is normal that the mean growth rate of a cell is higher than the growth rate between two microspheres because it reflects the overall growth of the cell which is the sum of local growth throughout the cell. The mean growth rate of caulonemal cells was 19.87±2.18 µm h–1 while chloronemal cells grew at 5.85±0.51 µm h–1 (Table 1). These values are within the range observed previously when mosses were grown on agar plates (Schmiedel and Schnepf, 1980; Duckett et al., 1998). This indicates that neither the microspheres nor the imaging conditions had a detrimental effect on cell growth.
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Microspheres can be used to identify diffuse growth in expanding cells
Since the aim of this study is to discriminate between tip growth and diffuse growth, it was necessary to show that the microsphere time lapse method can be used to identify and measure the rates of diffuse growth. To this end, the expansion of tobacco BY-2 cells from suspension cultures which undergo diffuse growth was imaged. The mean growth rate of the BY-2 cells was 0.9±0.14 µm h–1 (Table 1). It was observed that the distance between microspheres attached to all regions of the cell surface increases during the growth of the BY-2 cell (Fig. 2). For example, the growth rate between microspheres a and b was 0.16 µm h–1, and 0.29 µm h–1 between microspheres c and d (Fig 2). These observations indicate that growth is occurring over large areas of the surface of the cell. This growth pattern is characteristic of diffuse growth. Therefore, this experiment shows that the microspheres can be used to determine if a cell expands by diffuse growth.
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Caulonemal cells grow by tip growth
Caulonemal cells were unequivocally identified by their distinctive oblique cross wall (Figs 1, 3). Caulonema were labelled with microspheres and images were captured over periods of 24 h. A representative microsphere-labelled cell is shown in Fig. 3. Only the microspheres attached to the cell surface at the tip area (a and b) are displaced during the growth period. The microspheres move to the side of the cell and then stop moving relative to the growing tip. In contrast, those microspheres located along the side of the cell (c, d, e, and f) do not move relative to each other, i.e. they stay in the same position during cell growth. Precise measurement of cell growth in three different areas of the cell shows that growth is restricted to the tip of the cell, no growth being detected in the basal and intermediary zones (Table 2). The movement of microspheres from the tip to the sides of the cell during growth results in the tip regions being depleted of microspheres after 2 h. This results in the formation of a ‘dark’ tip without any microsphere relative to the fluorescent sides of the cell. The formation of such unlabelled regions at the apex of a tip-growing cell is diagnostic of tip growth. The tip growth pattern shown in Fig. 2 was found in all cells that were imaged (n=11; Table 1). The mean growth rate of caulonemal cells was 19.87±2.18 µm h–1.
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Chloronemal cells grow by tip growth
Chloronemal cells were identified by the presence of transverse cross walls perpendicular to the axis of growth and the abundance of large chloroplasts (Figs 1, 4). The mean growth rate of chloronemal cells was 5.8±0.51 µm h–1 (Table 1). This is less than the growth rate of caulonemal cells (above). The formation of a ‘dark’ zone at the chloronemal tip indicates that growth is restricted to the apical region of the cell, as demonstrated above for caulonema (Fig. 4). Microspheres at the tip of the cell (a and b) separated at a rate of 4.1 µm h–1, while the microspheres on the side of the cells (c, d, e, and f) maintained a constant separation indicating that growth was restricted to the tip and was absent from the sides of the cells (Table 2). No diffuse growth was detected in the basal area of chloronemal cells, demonstrating that these cells, despite their slow speed of growth, are exclusively growing by tip growth (Fig. 4; Table 2). This result was confirmed with other chloronemal cells (n=25) (Table 1). A movie showing eight well-labelled growing chloronemal cells is available in the Supplementary material at JXB online. This indicates that chloronemal cells expand by tip growth exclusively, and diffuse growth does not contribute to their expansion.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Here time-lapse imaging was used to show that both chloronemal and caulonemal cells expand by tip growth. The method used to discriminate between diffuse growth and tip growth is unambiguous because the occurrence of growth can be identified along the entire surface of the cell. Control experiments with expanding BY-2 cells, which are known to grow by diffuse growth, show that this method can detect the occurrence of this mode of growth. Furthermore, this method has been used to localize and measure local growth rates in tip-growing root hairs (Shaw et al., 2000). While the present analysis confirms that caulonemal cells expand by tip growth, this is the first clear demonstration that chloronemal cells expand exclusively by tip growth and not by diffuse growth. This clarifies an uncertainty that has existed in the literature for some time (see detailed evaluation of previous studies by Duckett et al., 1998). It also shows that a relatively slow growth rate and the absence of a clear tip body are not good criteria to determine that a cell type is growing by diffuse growth instead of tip growth.
While both caulonemal and chloronemal cells expand by tip growth, there is clear evidence that their growth processes are different. The tip growth of caulonemal cells is similar to the tip growth observed in root hairs and pollen tubes where there is an accumulation of cytoplasm at the tip (Schmiedel and Schnepf, 1980; Carol and Dolan, 2002). In contrast, the growth of the chloronemal tip is relatively slow and there is no evidence for the formation of a tip body, and in some instances a very thin layer of cytoplasm which may contain large chloroplasts lines the tip (Duckett et al., 1998). Ultrastuctural analyses of the growing tip of chloronemal cells of Dawsonia superba (Polytrichaceae) and Funaria hygrometrica (a member of the Funariales, like P. patens) have shown that there is no tip body in the apex like that present in the tip of caulonemal cells (Demaggio and Stetler, 1977; Schmiedel and Schnepf, 1979). Dictyosomes and Golgi vesicles were observed in both species, but they did not accumulate at the tip of the chloronemal cell as they did in caulonema (Schmiedel and Schnepf, 1980). Thus the cytology of the growing tips indicates that there may be differences in the mechanisms by which tip growth is achieved in chloronema and caulonema. Further characterization of the growth mechanism of these cells will define the differences between chloronemal and caulonemal tip growth.
Despite the morphological differences between chloronemal and caulonemal cells, there is evidence of proteins that are involved in the growth of both cell types. For example, a group of arabinogalactan-rich glycoproteins and members of the actin-related protein 2/3 complex (ARPC) have been found to be involved in both chloronemal and caulonemal growth, indicating that there are some common features between the two kinds of tip growth (Harries et al., 2005; Lee et al., 2005; Perroud and Quatrano, 2006). RNA interference of the ARPC1 subunit dramatically reduces the growth rate of chloronemal cells and totally inhibits the formation of caulonemal cells (Harries et al., 2005). Mutants of another ARPC subunit (ARPC4) are slightly less defective in chloronemal growth but also fail to develop caulonema (Perroud and Quatrano, 2006). ARPC4 was shown to localize at the tip of caulonemal cells, confirming its function in caulonemal tip growth, but its localization in chloronema was not reported (Perroud and Quatrano, 2006). Thus the ARPC complex is required for both chloronemal and caulonemal tip growth, but is more important for caulonemal growth. Arabinogalactan proteins (AGPs) are also required for both modes of tip growth. Treatment of Physcomitrella protonema with a reagent that binds to AGPs completely arrests the growth of both chloronemal and caulonemal cells (Lee et al., 2005). Furthermore, Physcomitrella mutants that lack one of ten putative Physcomitrella AGPs have slightly shorter chloronemal and caulonemal cells than wild-type moss. AGP proteins are present at the plasma membrane throughout the surface of chloronemal cells, but they are particularly abundant in the cell wall region of the tip (Lee et al., 2005). This tip accumulation is consistent with a function for AGPs in chloronemal tip growth and suggests that AGPs are required for new cell wall formation in these cells. Together, these data indicate that despite morphological and growth rate differences, there are proteins that are involved in both types of tip growth, indicating that there may be a common molecular mechanism that affects growth. A full understanding of the molecular, cellular, and physiological differences between chloronemal and caulonemal tip growth is central to understanding the elaboration of this part of the moss body.
Supplementary material
Supplementary movie 1, available at JXB online, is a time-lapse movie of fluorescent microsphere movement on the surface of eight chloronemal cells. Cells labelled at their tip are indicated by a number (1–8). Overlay of bright field (red) and fluorescent field (green). Scale bar=50 µm.
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Acknowledgements |
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We are grateful to Mario Izaguirre-Sierra, Monica Pernas-Ochoa, Seiji Takeda, and Keke Yi for their critical comments on the manuscript. This research is funded by a grant from NERC (Ne/c510732/1) to LD and a grant in aid from BBSRC to the John Innes Centre.
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References |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Ashton NW, Cove DJ. Isolation and preliminary characterization of auxotrophic and analog resistant mutants of moss, Physcomitrella patens. Molecular and General Genetics (1977) 154:87–95.[CrossRef]
Ashton NW, Grimsley NH, Cove DJ. Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta (1979) 144:427–435.[CrossRef][Web of Science]
Braun M. Gravitropism in tip-growing cells. Planta (1997) 203:S11–S19.[CrossRef][Web of Science][Medline]
Braun M, Hauslage J, Czogalla A, Limbach C. Tip-localized actin polymerization and remodeling, reflected by the localization of ADF, profilin and villin, are fundamental for gravity-sensing and polar growth in characean rhizoids. Planta (2004) 219:379–388.[CrossRef][Web of Science][Medline]
Carol RJ, Dolan L. Building a hair: tip growth in Arabidopsis thaliana root hairs. Philosophical Transactions of the Royal Society B: Biological Sciences (2002) 357:815–821.[CrossRef]
Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H, Derbyshire P, Drea S, Zarsky V, Dolan L. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature (2005) 438:1013–1016.[CrossRef][Medline]
Chan J, Calder G, Fox S, Lloyd C. Localization of the microtubule end binding protein EB1 reveals alternative pathways of spindle development in Arabidopsis suspension cells. The Plant Cell (2005) 17:1737–1748.
Cove D. The moss Physcomitrella patens. Annual Review of Genetics (2005) 39:339–358.[CrossRef][Web of Science][Medline]
Davis P, Kenrick P. Fossil plants (2004) London: The Natural History Museum.
Demaggio AE, Stetler DA. Protonemal organization and growth in moss Dawsonia superba—ultrastructural characteristics. American Journal of Botany (1977) 64:449–454.[CrossRef][Web of Science]
Doonan JH, Cove DJ, Lloyd CW. Immunofluorescence microscopy of microtubules in intact cell lineages of the moss, Physcomitrella patens. 1. Normal and CIPC-treated tip cells. Journal of Cell Science (1985) 75:131–147.[Abstract]
Duckett JG, Schmid AM, Ligrone R. Protonemal morphogenesis. In: Bryology for the twenty-first century—Bates JW, Ashton NW, Duckett JG, eds. (1998) London: British Bryological Society. 223–245.
Foreman J, Demidchik V, Bothwell JHF, et al. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature (2003) 422:442–446.[CrossRef][Medline]
Gu Y, Fu Y, Dowd P, Li SD, Vernoud V, Gilroy S, Yang ZB. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. Journal of Cell Biology (2005) 169:127–138.
Harries PA, Pan A, Quatrano RS. Actin-related protein2/3 complex component ARPC1 is required for proper cell morphogenesis and polarized cell growth in Physcomitrella patens. The Plant Cell (2005) 17:2327–2339.
Horio T, Oakley BR. The role of microtubules in rapid hyphal tip growth of Aspergillus nidulans. Molecular Biology of the Cell (2005) 16:918–926.
Katsaros C, Karyophyllis D, Galatis B. Cytoskeleton and morphogenesis in brown algae. Annals of Botany (2006) 97:679–693.
Lee KJ, Sakata Y, Mau SL, Pettolino F, Bacic A, Quatrano RS, Knight CD, Knox JP. Arabinogalactan proteins are required for apical cell extension in the moss Physcomitrella patens. The Plant Cell (2005) 17:3051–3065.
Nagata T, Nemoto Y, Hasezawa S. Tobacco BY-2 cell-line as the HeLa cell in the cell biology of higher-plants. International Review of Cytology (1992) 132:1–30.[Web of Science]
Perroud PF, Quatrano RS. The role of ARPC4 in tip growth and alignment of the polar axis in filaments of Physcomitrella patens. Cell Motility and the Cytoskeleton (2006) 63:162–171.[CrossRef][Web of Science][Medline]
Reiss HD, Herth W. Calcium gradients in tip-growing plant cells visualized by chlorotetracycline fluorescence. Planta (1979) 146:615–621.[CrossRef][Web of Science]
Schmiedel G, Schnepf E. Side branch formation and orientation in the caulonema of the moss, Funaria hygrometrica—normal development and fine-structure. Protoplasma (1979) 100:367–383.[CrossRef][Web of Science]
Schmiedel G, Schnepf E. Polarity and growth of caulonema tip cells of the moss Funaria hygrometrica. Planta (1980) 147:405–413.[CrossRef][Web of Science]
Shaw SL, Dumais J, Long SR. Cell surface expansion in polarly growing root hairs of Medicago truncatula. Plant Physiology (2000) 124:959–970.
Smith LG. Cytoskeletal control of plant cell shape: getting the fine points. Current Opinion in Plant Biology (2003) 6:63–73.[CrossRef][Web of Science][Medline]
Tiwari SC, Wilkins TA. Cotton (Gossypium hirsutum) seed trichomes expand via diffuse growing mechanism. Canadian Journal of Botany–Revue Canadienne De Botanique (1995) 73:746–757.
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