A rice β-1,3-glucanase gene Osg1 is required for callose degradation in pollen development

Planta

Volumn 233, Issue 2, 2011, Pages 309-323

  Wan, Linglin ^a   Zha, Wenjun ^a   Cheng, Xiaoyan ^a   Liu, Chuan ^a   Lv, Lu ^a   Liu, Caixiang ^a   Wang, Zhanqi ^a   Du, Bo ^a   Chen, Rongzhi ^a   Zhu, Lili ^a   He, Guangcun ^a  

^a WUHAN UNIVERSITY   (China)

Author keywords

Callose; Male sterility; Pollen development; Rice (Oryza sativa); Tetrad; 1,3 Glucanase

Indexed keywords

ORYZA SATIVA;

EID: 79251470798     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1301-z     Document Type: Article

References (76)

1. Akiyama T, Pillai MA (2001) Molecular cloning, characterization and in vitro expression of a novel endo-1, 3-β-glucanase up-regulated by ABA and drought stress in rice (Oryza sativa L.). Plant Sci 161: 1089-1098. doi: 10. 1016/S0168-9452(01)00518-0.
2. Akiyama T, Kaku H, Shibuya N (1996) Purification and properties of a basic endo-1, 3-beta-glucanase from rice (Oryza sativa L.). Plant Cell Physiol 37: 702-705.
3. Akiyama T, Shibuya N, Hrmova M, Fincher GB (1997) Purification and characterization of a (1→3)-beta-d-glucan endohydrolase from rice (Oryza sativa) bran. Carbohydr Res 297: 365-374. doi: 10. 1016/S0168-9452(98)00032-6.
4. Akiyama T, Pillai MA, Sentoku N (2004) Cloning, characterization and expression of OsGLN2, a rice endo-1, 3-beta-glucanase gene regulated developmentally in flowers and hormonally in germinating seeds. Planta 220: 129-139. doi: 10. 1007/s00425-004-1312-8.
5. Akiyama T, Jin S, Yoshida M, Hoshino T, Opassiri R, Ketudat Cairns JR (2009) Expression of an endo-(1, 3; 1, 4)-beta-glucanase in response to wounding, methyl jasmonate, abscisic acid and ethephon in rice seedlings. J Plant Physiol 166: 1814-1825. doi: 10. 1016/j. jplph. 2009. 06. 002.
6. Bate N, Twell D (1998) Functional architecture of a late pollen promoter: pollen-specific transcription is developmentally regulated by multiple stage-specific and co-dependent activator elements. Plant Mol Biol 37: 859-869. doi: 10. 1023/A: 1006095023050.
7. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4: 879-887. doi: 10. 1105/tpc. 4. 8. 879.
8. Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60: 1465-1478. doi: 10. 1093/jxb/ern355.
9. Bucciaglia PA, Smith AG (1994) Cloning and characterization of Tag1, a tobacco anther β-1, 3-glucanase expressed during tetrad dissolution. Plant Mol Biol 24: 903-914. doi: 10. 1007/BF00014444.
10. Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1-30. doi: 10. 1111/j. 1365-313X. 1993. tb00007. x.
11. Carpita NC, McCann MC (2010) The maize mixed-linkage (1→3),(1→4)-β-d-glucan polysaccharide is synthesized at the Golgi membrane. Plant Physiol 153: 1362-1371. doi: 10. 1104/pp. 110. 156158.
12. Carpita NC, Defernez M, Findlay K, Wells B, Shoue DA., Catchpole G, Wilson RH, McCann MC (2001) Cell wall architecture of the elongating maize coleoptile. Plant Physiol 127: 551-565. doi: 10. 1104/pp. 010146.
13. Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 19: 847-861. doi: 10. 1105/tpc. 106. 044123.
14. Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5: 213-218. doi: 10. 1007/BF01969712.
15. Chye ML, Cheung KY (1995) Beta-1, 3-glucanase is highly-expressed in laticifers of Hevea brasiliensis. Plant Mol Biol 29: 397-402.
16. Cosgrove DJ (2005) Growth of the plant cell wall. Nature 6: 850-861. doi: 10. 1038/nrm1746.
17. De Loose M, Alliotte T, Gheysen G, Genetello C, Gielen J, Soetaert P, van Montagu M, Inze D (1988) Primary structure of a hormonally regulated beta-glucanase of Nicotiana plumbaginifolia. Gene 70: 13-23. doi: 10. 1016/0378-1119(88)90100-X.
18. Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42: 315-328. doi: 10. 1111/j. 1365-313X. 2005. 02379. x.
19. Du B, Zhang W, Liu B, Hu J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106: 22163-22168. doi: 10. 1073/pnas. 0912139106.
20. Eschrich W, Currier HB (1964) Identification of callose by its diachrome and fluorochrome reactions. Biotech Histochem 39: 303-307. doi: 10. 3109/10520296409061248.
21. Feng JH, Lu YG, Liu XD, Xu XB (2001) Pollen development and its stages in rice (Oryza sativa L.). Chin J Rice Sci 15: 21-28.
22. Filichkin SA, Leonard JM, Monteros A, Liu PP, Nonogaki H (2004) A novel endo-beta-mannanase gene in tomato LeMAN5 is associated with anther and pollen development. Plant Physiol 134: 1080-1087. doi: 10. 1104/pp. 103. 035998.
23. Fincher GB (2009) Revolutionary times in our understanding of cell wall biosynthesis and remodeling in the grasses. Plant Physiol 149: 27-37. doi: 10. 1104/pp. 108. 130096.
24. Hamilton DA, Schwarz YH, Mascarenhas JP (1998) A monocot pollen-specific promoter contains separable pollen-specific and quantitative elements. Plant Mol Biol 38: 663-669. doi: 10. 1023/A: 1006083725102.
25. Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146: 1810-1820. doi: 10. 1104/pp. 107. 111484.
26. 14C] thymidine derivatives during meiosis and microsporogenesis in Lilium anthers. J Cell Sci 2: 387-400.
27. Heyn ANJ (1969) Glucanase activity in coleoptiles of Avena. Arch Biochem Biophys 132: 442-449. doi: 10. 1016/0003-9861(69)90387-7.
28. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6: 271-282. doi: 10. 1046/j. 1365-313X. 1994. 6020271. x.
29. Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Res 27: 297-300.
30. Hird DL, Worrall D, Hodge R, Smartt S, Paul W, Scott R (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to beta-1, 3-glucanases. Plant J 4: 1023-1033. doi: 10. 1046/j. 1365-313X. 1993. 04061023. x.
31. Hoson T, Masuda Y, Nevins DJ (1992) Comparison of the outer and inner epidermis: inhibition of auxin-induced elongation of maize coleoptiles by glucan antibodies. Plant Physiol 98: 1298-1303.
32. Huang N, Wu L, Nandi S, Bowman E, Huang J, Sutliff T, Rodriguez RL (2001) The tissue-specific activity of a rice beta-glucanase promoter (Gns9) is used to select rice transformants. Plant Sci 161: 589-595. doi: 10. 1016/S0168-9452(01)00447-2.
33. Iglesias VA, Meins F Jr (2000) Movement of plant viruses is delayed in a β-1, 3-glucanase-deficient mutant showing a reduced plasmodesmatal size exclusion limit and enhanced callose deposition. Plant J 21: 157-166. doi: 10. 1046/j. 1365-313x. 2000. 00658. x.
34. Inouhe M, Nevins DJ (1991) Inhibition of auxin-induced cell elongation of maize coleoptiles by antibodies specific for cell wall glucanases. Plant Physiol 96: 426-431.
35. Itoh J, Nonomura K, Ikeda K, Yamaki S, Inukai Y, Yamagishi H, Kitano H, Nagato Y (2005) Rice plant development: from zygote to spikelet. Plant Cell Physiol 46: 23-47. doi: 10. 1093/pcp/pci501.
36. Jin W, Horner HT, Palmer RG (1997) Genetics and cytology of a new genic male-sterile soybean [Glycine max (L.) Merr]. Sex Plant Reprod 10: 13-21.
37. Labavitch JM (1981) Cell wall turnover in plant development. Ann Rev Plant Physiol 31: 385-406.
38. Labrador E, Nevins DJ (1989) An exo-β-d-glucanase derived from Zea coleoptile walls with a capacity to elicit cell elongation. Physiol Plant 77: 479-486. doi: 10. 1111/j. 1399-3054. 1989. tb05380. x.
39. 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, vol 3. CRC Press, Boca Raton, pp 49-76.
40. Levy A, Erlanger M, Rosenthal M, Epel BL (2007) A plasmodesmata-associated β-1, 3-glucanase in Arabidopsis. Plant J 49: 669-682. doi: 10. 1111/j. 1365-313X. 2006. 02986. x.
41. Linthorst HJM, van Loon LC (1991) Pathogenesis-related proteins of plants. Crit Rev Plant Sci 10: 123-150. doi: 10. 1080/07352689109382309.
42. -ΔΔCT method. Methods 25: 402-408. doi: 10. 1006/meth. 2001. 1262.
43. Lotan T, Ori N, Fluhr R (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1: 881-887. doi: 10. 1105/tpc. 1. 9. 881.
44. Lucas WJ, Olesinski A, Hull RJ, Haudenshield JS, Deom CM, Beachy RN, Wolf S (1993) Influence of the tobacco mosaic virus 30-kDa movement protein on carbon metabolism and photosynthate partitioning in transgenic tobacco plants. Planta 190: 88-96. doi: 10. 1007/BF00195679.
45. Luo H, Lee JY, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006) RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue-specific gene expression in different plant species. Plant Mol Biol 62: 397-408. doi: 10. 1007/s11103-006-9031-0.
46. Masuda Y (1968) Role of cell-wall-degrading enzymes in cell-wall loosening in oat coleoptile. Planta 83: 171-184. doi: 10. 1007/BF00385022.
47. Masuda Y, Yamamoto R (1970) Effect of auxin on β-1, 3-glucanase activity in Avena coleoptile. Dev Growth Differ 11: 287-296. doi: 10. 1111/j. 1440-169X. 1970. 00287. x.
48. McCormick S (1993) Male gametophyte development. Plant cell 5: 1265-1275.
49. Melchers LS, Sela-Buurlage MB, Vloemans SA, Woloshuk CP, Vanroekel JSC, Pen J, van den Elzen PJM, Cornelissen BJC (1993) Extracellular targeting of the vacuolar tobacco proteins AP24, chitinase and β-1, 3-glucanase in transgenic plants. Plant Mol Biol 21: 583-593. doi: 10. 1007/BF00014542.
50. Memelink J, Linthorst HJ, Schilperoort RA, Hoge JH (1990) Tobacco genes encoding acidic and basic isoforms of pathogenesis-related proteins display different expression patterns. Plant Mol Biol 14: 119-126. doi: 10. 1007/BF00018553.
51. Nakamura K, Matsuoka K (1993) Protein targeting to the vacuole in plant cells. Plant Physiol 101: 1-5.
52. Neale AD, Wahleithner JA, Lund M, Bonnett HT, Kelly A, Meeks-Wagner DR, Peacock WJ, Dennis ES (1990) Chitinase, beta-1, 3-glucanase, osmotin, and extensin are expressed in tobacco explants during flower formation. Plant Cell 2: 673-684. doi: 10. 1105/tpc. 2. 7. 673.
53. Nishizawa Y, Saruta M, Nakazono K, Nishio Z, Soma M, Yoshida T, Nakajima E, Hibi T (2003) Characterization of transgenic rice plants over-expressing the stress-inducible beta-glucanase gene Gns1. Plant Mol Biol 51: 143-152. doi: 10. 1023/A: 1020714426540.
54. Parish RW, Li SF (2010) Death of a tapetum: a programme of developmental altruism. Plant Sci 178: 73-89. doi: 10. 1016/j. plantsci. 2009. 11. 001.
55. Rinne PLH et al (2005) Tobacco plants respond to the constitutive expression of the tospovirus movement protein NSM with a heat-reversible sealing of plasmodesmata that impairs development. Plant J 43: 688-707. doi: 10. 1111/j. 1365-313X. 2005. 02489. x.
56. Roberts AG, Oparka KJ (2003) Plasmodesmata and the control of symplastic transport. Plant Cell Environ 26: 103-124. doi: 10. 1046/j. 1365-3040. 2003. 00950. x.
57. Rogers HJ, Bate N, Combe J, Sullivan J, Sweetman J, Swan C, Lonsdale DM, Twell D (2001) Functional analysis of cis-regulatory elements within the promoter of the tobacco late pollen gene g10. Plant Mol Biol 45: 577-585. doi: 10. 1023/A: 1010695226241.
58. Romero GO, Simmons C, Yaneshita M, Doan M, Thomas BR, Rodriguez RL (1998) Characterization of rice endo-beta-glucanase genes (Gns2-Gns14) defines a new subgroup within the gene family. Gene 223: 311-320. doi: 10. 1016/S0378-1119(98)00368-0.
59. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, vol 1, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 31-45.
60. Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16(Suppl): S46-S60. doi: 10. 1105/tpc. 017012.
61. Shamay I, Rafael F (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. doi: 10. 1007/BF00277751.
62. Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19: 2064-2076. doi: 10. 1105/tpc. 106. 046250.
63. Simmons CR, Litts JC, Huang N, Rodriguez RL (1992) Structure of a rice beta-glucanase gene regulated by ethylene, cytokinin, wounding, salicylic acid and fungal elicitors. Plant Mol Biol 18: 33-45. doi: 10. 1007/BF00018454.
64. Steiglitz H, Stern H (1973) Regulation of β-1, 3-glucanase activity in developing anthers of Lilium. Dev Biol 34: 169-173. doi: 10. 1016/0012-1606(73)90347-3.
65. Stone BA, Clarke AE (1992) Chemistry and physiology of higher plant 1, 3-β-glucans (callose). In: Stone BA, Clarke AE (eds) Chemistry and biology of (1-3)-β-glucans. La Trobe University Press, Bundoora, pp 365-429.
66. Takeuchi Y, Yoshikawa M, Takeba G, Tanaka K, Shibata D, Horino O (1990) Molecular cloning and ethylene induction of mRNA encoding a phytoalexin elicitor-releasing factor, beta-1, 3-endoglucanase, in soybean. Plant Physiol 93: 673-682.
67. Thomas BR et al (2000) Endo-1, 3; 1, 4-β-glucanase from coleoptiles of rice and maize: role in the regulation of plant growth. Int J Biol Macromol 27: 145-149. doi: 10. 1016/S0141-8130(00)00110-0.
68. Twell D, Yamaguchi J, Wing RA, Ushiba J, McCormick S (1991) Promoter analysis of genes that are coordinately expressed during pollen development reveals pollen-specific enhancer sequences and shared regulatory elements. Genes Dev 5: 496-507. doi: 10. 1101/gad. 5. 3. 496.
69. Warmke HE, Overman MA (1972) Cytoplasmic male sterility in sorghum: I. Callose behavior in fertile and sterile anthers. J Hered 63: 103-108.
70. Waterkeyn L (1962) Les parois microsporocytaires de nature callosique chez Helleborus et Fadescantia. Cellule 62: 225-255.
71. Wesley SV, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, Singh SP, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG, Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J 27: 581-590. doi: 10. 1046/j. 1365-313X. 2001. 01105. x.
72. Wessels JGH, Sietsma JH (1981) Fungal cell wall: a survey. In: Tanner W, Loewus FA (eds) Encyclopedia of plant physiology, vol 13B. Springer, Berlin, pp 352-394.
73. 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. doi: 10. 1105/tpc. 4. 7. 759.
74. Wu HM, Cheun AY (2000) Programmed cell death in plant reproduction. Plant Mol Biol 44: 267-281. doi: 10. 1023/A: 1026536324081.
75. Yamaguchi T, Nakayama K, Hayashi T, Tanaka Y, Koike S (2002) Molecular cloning and characterization of a novel beta-1, 3-glucanase gene from rice. Biosci Biotechnol Biochem 66: 1403-1406. doi: 10. 1271/bbb. 66. 1403.
76. Yamamoto R, Nevins DJ (1981) Coleoptile growth-inducing capacities of exo-β-(1→3)-glucanases from fungi. Physiol Plant 51: 118-122. doi: 10. 1111/j. 1399-3054. 1981. tb00888. x.