Characterization of callase (β-1,3-d-glucanase) activity during microsporogenesis in the sterile anthers of Allium sativum L. and the fertile anthers of A. atropurpureum
Tóm tắt
We examined callase activity in anthers of sterile Allium sativum (garlic) and fertile Allium atropurpureum. In A. sativum, a species that produces sterile pollen and propagates only vegetatively, callase was extracted from the thick walls of A. sativum microspore tetrads exhibited maximum activity at pH 4.8, and the corresponding in vivo values ranged from 4.5 to 5.0. Once microspores were released, in vitro callase activity peaked at three distinct pH values, reflecting the presence of three callase isoforms. One isoform, which was previously identified in the tetrad stage, displayed maximum activity at pH 4.8, and the remaining two isoforms, which were novel, were most active at pH 6.0 and 7.3. The corresponding in vivo values ranged from pH 4.75 to 6.0. In contrast, in A. atropurpureum, a sexually propagating species, three callase isoforms, active at pH 4.8–5.2, 6.1, and 7.3, were identified in samples of microsporangia that had released their microspores. The corresponding in vivo value for this plant was 5.9. The callose wall persists around A. sativum meiotic cells, whereas only one callase isoform, with an optimum activity of pH 4.8, is active in the acidic environment of the microsporangium. However, this isoform is degraded when the pH rises to 6.0 and two other callase isoforms, maximally active at pH 6.0 and 7.3, appear. Thus, factors that alter the pH of the microsporangium may indirectly affect the male gametophyte development by modulating the activity of callase and thereby regulating the degradation of the callose wall.
Tài liệu tham khảo
Abad AR, Mehrtens BJ, Mackenzie SA (1995) Specific expression in reproductive tissue and fate of mitochondrial sterility-associated protein in cytoplasmic male-sterile bean. Plant Cell 7:271–285
Armitage P, Berry G (1987) Statistical methods in medical research. Blackwell, Oxford
Bhandari NN, Bhargava M, Geier T (1981) A persisting cellulosic wall of microspore mother cells during microsporogenesis in Allium tuberosum Rottl. and Cyclamen persicum Mill. Ann Bot 48:425–431
Chebli Y, Geitmann A (2007) Mechanical principles governing pollen tube growth. Funct Plant Sci Biotech 1:232–245
Chen XY, Kim JY (2009) Callose synthesis in higher plants. Plant Signal Behav 4:489–492
Curtis IS, Caiping H, Scott RJ, Power JB, Davey MR (1996) Genomic male sterility in lettuce a baseline for the production of F1 hybrids. Plant Sci 113:113–119
Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DPS (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328
Dong X, Hong Z, Chatterjee J, Kim S, Verma DPS (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87–98
Elemo GN, Elemo BO, Erukainure OL (2011) Activities of some enzymes, enzyme inhibitors and antinutritional factors from the seeds of sponge gourd (Luffa aegyptiaca M.). Afr J Biochem Res 5:86–89
Engelke T, Hülsmann S, Tatlioglu T (2002) A comparative study of microsporogenesis and anther wall development in different types of genic and cytoplasmic male sterilities in chives. Plant Breeding 121:254–258
Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE (2005) Two callose synthases GSL1 and GSL5 play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 58:333–349
Fei H, Sawhney VK (1999) MS32-regulated timing of callose degradation during microsporogenesis in Arabidopsis is associated with the accumulation of stacked rough ER in tapetal cells. Sex Plant Reprod 12:188–193
Frankel R, Izhar S, Nitsan J (1969) Timing of callase activity and cytoplasmic male sterility in Petunia. Biochem Genet 3:451–455
Furness CA, Rudall PJ (1999) Microsporogenesis in monocotyledons. Ann Bot 84:475–499
Gomez–Gomez L, Boller T (2002) Flagellin perception: a paradigm for innate immunity. Trends Plant Sci 7:251–256
Gori P (1983) Ultrastructural changes in the wall of the sporogenous cells in Allium sativum clone Piemonte during microsporogenesis. Ann Bot 51:139–143
Hong Z, Delauney AJ, Verma DPS (2001) A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 13:755–768
Izhar S, Frankel R (1971) Mechanism of male sterility in Petunia: the relationship between pH, callase activity in the anthers and the breakdown of the microsporogenesis. Theor Appl Genet 41:104–108
Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase GSL5 is required for wound and papillary callose formation. Plant Cell 15:2503–2513
Jensen WA (1962) Botanical histochemistry. Freeman and Co., San Francisco
Jin W, Horner HT, Reid G, Shoemaker RC (1999) Analysis and mapping of gene families encoding β-13-glucanases of soybean. Genetics 153:445–452
Krabel D, Eschrich W, Wirth S, Wolf G (1993) Callase (1,3-Beta-D-glucanase) activity during spring reaction in deciduous trees. Plant Sci 93:19–23
Laitiainen E, Nieminen KM, Vihinen H, Raudaskoski M (2002) Movement of generative cell and vegetative nucleus in tobacco pollen tubes is dependent on microtubule cytoskeleton but independent of the synthesis of callose plugs. Sex Plant Reprod 15:195–204
Leubner-Metzger G, Meins F Jr (1999) Functions and regulation of plant β-1,3-glucanases (PR-2). In: Datta SK, Muthukrishnan S (eds) Pathogenesis-related proteins in plants. CRC Press, Boca Raton, pp 49–76
Li T, Gong C, Wang T (2010) RA68 is required for postmeiotic pollen development in Oryza sativa. Plant Mol Biol 72:265–277
Majewska-Sawka A, Rodriguez-Garcia M (1999) The special callose wall: a new insight. In: Clement C, Pacini E, Audran J (eds) Anther and pollen: from biology to biotechnology. Springer, Heidelberg, pp 119–127
Malhó R (2006) The pollen tube: a cellular and molecular perspective. Springer, Berlin
Mamun EA, Cantrill LC, Overall RL, Sutton BG (2005) Cellular organisation in meiotic and early post-meiotic rice anthers. Cell Biol Int 29:903–913
McCormick S (1993) Male gametophyte development. Plant Cell 5:1265–1275
Mepham RH, Lane GR (1969) Formation and development of the tapetal periplasmodium in Tradescantia bracteata. Protoplasma 68:175–192
Mollet JC, Kim S, Jauh GY, Lord EM (2002) Arabinogalactan proteins, pollen tube growth and the reversible effects of Yariv phenylglycoside. Protoplasma 219:89–98
Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972
Pacini E (1990) Tapetum and microspore function. In: Blackmore S, Knox RB (eds) Microspores: evolution and ontogeny. Academic Press, San Diego, pp 213–237
Periasamy K, Amalathas J (1991) Absence of callose and tetrad in microsporogenesis of Pandanus odoratissimus with well-formed pollen exine. Ann Bot 67:29–33
Reynolds ES (1963) The use of the lead citrate of high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Rodriguez-Garcia MI, Majewska-Sawka A (2011) Is the special callose wall of microsporocytes an impermeable barrier? J Exp Bot 12:1659–1663
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:46–60
Sexton R, Del Campillo E, Duncan D, Lewis LN (1990) The purification of an anther cellulase (β(1:4)4-glucan hydrolase) from Lathyrus odoratus L. and its relationship to the similar enzyme found in abscission zones. Plant Sci 67:169–176
Shivaraj B, Pattabiraman TN (1981) Natural plant enzyme inhibitors. Characterization of an unusual a-amylase/trypsin inhibitor from ragi (Eleusine coracana Geartn). Biochem J 193:29–36
Stieglitz H (1977) Role of β-1,3-glucanase in postmeiotic microspore release. Dev Biol 58:87–97
Stieglitz H, Stern H (1973) Regulation of β-1,3-glucanase activity in developing anthers of Lilium. Dev Biol 34:169–173
Stone BA, Clarke AE (1992) Chemistry and biology of (1,3)-β-D-glucans. La Trobe University Press, Victoria
Teng N, Huang Z, Mu X, Jin B, Hu Y, Lin J (2005) Microsporogenesis and pollen development in Leymus chinensis with emphasis on dynamic changes in callose deposition. Flora 3:256–263
Trebacz K (1992) Measurement of intra- and extracellular pH in the liverwort Conocephalum conicum during action potentials. Physiol Plant 84:448–452
Vervaeke I, Londers E, Piot G, Deroose R, Proft MPD (2005) The division of the generative nucleus and the formation of callose plugs in pollen tubes of Aechmea fasciata (Bromeliaceae) cultured in vitro. Sex Plant Reprod 18:9–19
Wan L, Zha W, Cheng X, Liu C, Lv L, Liu C, Wang Z, Du B, Chen R, Zhu L, He G (2011) A rice β-1,3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta 233:309–323
Waterkeyn L, Bienfail A (1970) On a possible function of the callosic special wall in Ipomea purpurea (L.) Roth. Grana 10:13–20
Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R (1992) Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4:759–771
Wu FS, Murry LE (1985) Proteolytic activity in anther extracts of fertile and cytoplasmic male sterile petunia. Plant Physiol 79:301–305
Xie B, Wang X, Hong Z (2010) Precocious pollen germination in Arabidopsis plants with altered callose deposition during microsporogenesis. Planta 231:809–823
Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG (2003) TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 34:229–240