Summary
Within the infected cells of root nodules there is evidence of stratification and organisation of symbiosomes and other organelles. This organisation is likely to be important for the efficient exchange of nutrients and metabolites during functioning of the nodules. Using immunocytochemical labelling and confocal microscopy we have determined the organisation of cytoskeletal elements, micro tubules and actin microfilaments in soybean nodule cells, with a view to assessing their possible role in organelle distribution. Most microtubule arrays occurred in the cell cortex where they formed disorganised arrays in both uninfected and infected cells from mature nodules. In infected cells from developing nodules, parallel arrays of microtubules, transverse to the long axis of the cell, were observed. In incipient nodules, before release of rhizobia into the plant cells, the cells also had an array of microtubules which radiated from the nucleus into the cytoplasm. Three actin arrays were identified in the infected cells of mature nodules: an aster-like array which emanated from the surface of the nucleus, a cortical array which had an arrangement similar to that of the cortical microtubules, and, throughout the cytoplasm, an array of fine filaments which had a honeycomb arrangement consistent with a distribution between adjacent symbiosomes. Uninfected cells from mature nodules had only a random cortical array of actin filaments. In incipient nodules, the density of actin microfilaments associated with the nucleus and radiating through the cytoplasm was much less than that seen in mature infected cells. The cortical array of actin also differed, being composed of swirling configurations of filaments. After invasion of nodule cells by the rhizobia, the number of actin filaments emanating from the nucleus increased markedly and formed a network through the cytoplasm. Conversely, the cytoplasmic array in uninfected cells of developing nodules was identical to that in the cells of incipient nodules. The cytoplasmic network in infected cells of developing nodules is likely to be the precursor of the honeycomb array seen in mature nodule cells. We propose that this actin array plays a role in the spatial organisation of symbiosomes and that the microtubules are involved in the localisation of mitochondria and plastids at the cell periphery in the infected cells of root nodules.
Similar content being viewed by others
References
Abe S, You W, Davies E (1991) Protein bodies in corn endosperm are enclosed by and enmeshed in F-actin. Protoplasma 165: 139–149
Bergersen FJ (1958) The bacterial component of soybean root nodules: changes in respiratory activity, cell dry weight and nucleic acid content with increasing nodule age. J Gen Microbiol 19: 312–323
Bergersen FJ (1997) Physiological and biochemical aspects of nitrogen fixation by bacteroids in soybean nodule cells. Soil Biol Biochem 29: 875–880
Chida Y, Ueda K (1992) Detection of actin on organelles ofTrebouxia potteri, in particular on the surface of lysosomes. Protoplasma 171: 28–33
Cho S-O, Wick SM (1991) Actin in the developing stomatal complex of winter rye: a comparison of actin antibodies and Rh-phalloidin labeling of control and CB-treated tissues. Cell Motil Cytoskeleton 19: 25–36
Clayton L, Lloyd CW (1985) Actin organisation during the cell cycle in meristematic plant cells. Exp Cell Res 156: 231–238
Cleary AL, Mathesius U (1996) Rearrangements of F-actin during stomatogenesis visualised by confocal microscopy in fixed and permeabilisedTradescantia leaf epidermis. Bot Acta 109: 15–24
Clore AM, Dannenhoffer JM, Larkins BA (1996) EF-1 is associated with a cytoskeletal network surrounding protein bodies in maize endosperm cells. Plant Cell 8: 2003–2014
Cyr RJ (1994) Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol 10: 153–180
Dong X-J, Ryu J-H, Takagi S, Nagai R (1996) Dynamic changes in the organisation of microfilaments associated with photocontrolled motility of chloroplasts in epidermal cells ofVallisneria. Protoplasma 195: 18–24
Foissner I, Lichtscheidl IK, Wasteneys GO (1996) Actin-based vesicle dynamics and exocytosis during wound wall formation in characean internodal cells. Cell Motil Cytoskeleton 35: 35–48
Goodbody KC, Lloyd CW (1990) Actin filaments line up acrossTradescantia epidermal cells, anticipating wound-induced division planes. Protoplasma 157: 92–101
Goodchild DJ, Bergersen FJ (1966) Electron microscopy of the infection and subsequent development of soybean nodule cells. J Bacteriol 92: 204–213
Gunning BES, Hardham AR (1982) Microtubules. Annu Rev Plant Physiol 33: 651–698
Hanks JF, Schubert KR, Tolbert NE (1983) Isolation and characterisation of infected and uninfected cells from soybean nodules. Plant Physiol 71: 869–873
Hardham AR (1982) Regulation of polarity in tissues and organs. In: Lloyd CW (eds) The Cytoskeleton in plant growth and development. Academic Press, London, pp 377–403
Heath IB (1994) The Cytoskeleton in hyphal growth, organelle movements, and mitosis. In: Wessels JGH, Meinhardt F (eds) The mycota I: growth, differentiation and sexuality. Springer, Berlin Heidelberg New York Tokyo, pp 43–65
Herr FB, Heath MC (1982) The effects of antimicrotubule agents on organelle positioning in the cowpea rust fungus,Uromyces phaseoli var. Vignae. Exp Mycol 6: 15–24
Howard RJ, Aist JR (1977) Effects of MBC on hyphal tip organization, growth, and mitosis ofFusarium acuminatum, and their antagonism by D2O. Protoplasma 92: 195–210
Hunt S, King BJ, Canvin DT, Layzell DB (1987) Steady and nonsteady state gas exchange characteristics of soybean nodules in relation to the oxygen diffusion barrier. Plant Physiol 84: 164–172
Hyde GJ, Hardham AR (1993) Microtubules regulate the generation of polarity in zoospores ofPhytophthora cinnamomi. Eur J Cell Biol 62: 75–85
Kadota A, Wada M (1989) Photoinhibition of circular F-actin on chloroplast in a fern protonemal cell. Protoplasma 151: 171–174
Kakimoto T, Shibaoka H (1987) Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140: 151–156
Lancelle SA, Hepler PK (1988) Cytochalasin-induced ultrastructural alterations in Nicotiana pollen tubes. Protoplasma Suppl 2: 65–75
Langestein B, Silvester WB, Berg RH (1997) Microtubule-mediated function in a plant symbiosis. In: Proceedings of 16th annual symposium: current topics in plant biochemistry, physiology and molecular biology, Missouri, April 16–19, 1997
Lichtscheidl IK, Lancelle SA, Hepler PK (1990) Actin-endoplasmic reticulum complexesin Drosera. Protoplasma 155: 116–126
Menzel D, Schliwa M (1986) Motility in the siphonous green algaBryopsis II: chloroplast movement requires organized arrays of both microtubules and actin filaments. Eur J Cell Biol 40: 286–295
Millar AH, Day DA, Bergersen FJ (1995) Microaerobic respiration and oxidative phosphorylation by soybean nodule mitochondria: implications for nitrogen fixation. Plant Cell Environ 18: 715–726
Miyake T, Hasezawa S, Nagata T (1997) Role of cytoskeletal components in the migration of nuclei during the cell cycle transition from g1 phase to S phase of tobacco BY-2 cells. J Plant Physiol 150: 528–536
Mylona P, Pawlowski K, Bisseling T (1995) Symbiotic nitrogen fixation. Plant Cell 7: 869–885
Newcomb W (1981) Nodule morphogenesis and differentiation. Int Rev Cytol Suppl 13: 247–298
— (1985) Ultrastructural specialisation for ureide production in uninfected cells of soybean root nodules. Protoplasma 125: 1–12
Panteris E, Apostolakos P, Galatis B (1992) The organization of Factin in the root tip cells ofAdiantum capillus veneris throughout the cell cycle. Protoplasma 170: 128–137
Parthasarathy MV (1985) F-actin architecture in coleoptile epidermal cells. Eur J Cell Biol 39: 1–12
Perez HE, Sanchez N, Vidali L, Hernandez JM, Lara M, Sanchez F (1994) Actin isoforms in noninfected roots and symbiotic root nodules ofPhaseolus vulagris L. Planta 193: 51–56
Price GD, Day DA, Gresshoff PM (1987) Rapid isolation of intact peribacteroid envelopes from soybean nodules and demonstration of selective permeability to metabolites. J Plant Physiol 130: 157–164
Roth E, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49: 13–23
—, Jeon K, Stacey G (1988) Homology on endosymbiotic systems: the term “symbiosome”. In: Palacios R, Verma DPS (eds) Molecular genetics of plant-microbe interactions. American Phytopathology Society, St Paul, pp 220–225
Satiat-Jeunemaitre B, Steele C, Hawes C (1996) Golgi-membrane dynamics are Cytoskeleton dependent: a study on Golgi stack movement induced by brefeldin A. Protoplasma 191: 21–33
Schelp BJ, Atkins CA, Storer PJ, Canvin DT (1983) Cellular and subcellular organisation of pathways of ammonia assimilation and ureide synthesis in nodules of cowpea (Vigna unguiculata L. Walp). Arch Biochem Biophys 224: 429–441
Seagull RW, Falconer MM, Weerdenburg CA (1987) Microfilaments: dynamic arrays in higher plant cells. J Cell Biol 104: 995–1004
Selker JM (1988) Three-dimensional organization of uninfected tissue in soybean root nodules and its relation to cell specialization in the central region. Protoplasma 147: 178–190
—, Newcomb EH (1985) Spatial relationships between uninfected and infected cells in root nodules of soybean. Planta 165: 446–454
Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plants visualised by rhodamine phalloidin after pretreatment with m-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86
Staiger CJ, Schliwa M (1987) Actin localisation and function in higher plants. Protoplasma 141: 1–12
Streeter JG (1991) Transport and metabolism of carbon and nitrogen in legume nodules. Adv Bot Res 18: 129–187
Tanaka I (1991) Microtubule-determined plastid distribution during microsporogenesis inLilium longiflorum. J Cell Sci 99: 21–31
Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395
Vance CP, Heichel GH (1991) Carbon in N2 fixation: limitation or exquisite adaptation. Annu Rev Plant Physiol Plant Mol Biol 42: 373–392
Vidali L, Perez HE, Lopez VV, Noguez R, Zamudio F, Sanchez F (1995) Purification, characterisation and cDNA cloning of profilm fromPhaseolus vulgaris. Plant Physiol 108: 115–123
Walker LM, Sack FD (1995) Microfilament distribution in protonemata of the mossCeratodon. Protoplasma 189: 229–237
Wasteneys GO, Williamson RE (1987) Microtubule orientation in developing internodal cells ofNitella: a quantitative analysis. Eur J Cell Biol 43: 14–22
— — (1991) Endoplasmic microtubules and nucleus-associated actin rings inNitella internodal cells. Protoplasma 162: 86–98
— — (1993) Cortical microtubule organization and internodal cell maturation inChara corallina. Bot Acta 106: 136–142
—, Collings DA, Gunning BBS, Hepler PK, Menzel D (1996) Actin in living and fixed characean internodal cells: identification of a cortical array of fine actin strands and chloroplast actin rings. Protoplasma 190: 25–38
Whitehead LF, Day DA (1997) The peribacteroid membrane. Physiol Plant 100: 30–44
Williamson RE (1980) Actin in motile and other processes in plant cells. Can J Bot 58: 766–772
— (1993) Organelle movements. Annu Rev Plant Physiol Plant Mol Biol 44: 181–202
Yaffe MP, Harata D, Verde F, Eddison M, Toda T, Nurse P (1996) Microtubules mediate mitochondrial distribution in fission yeast. Proc Natl Acad Sci USA 93: 11664–11668
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Whitehead, L.F., Day, D.A. & Hardham, A.R. Cytoskeletal arrays in the cells of soybean root nodules: The role of actin microfilaments in the organisation of symbiosomes. Protoplasma 203, 194–205 (1998). https://doi.org/10.1007/BF01279476
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01279476