A chimeric arabinogalactan protein promotes somatic embryogenesis in cotton cell culture

Plant Physiology

Volumn 160, Issue 2, 2012, Pages 684-695

  Poon, Simon ^a,b   Heath, Robyn Louise ^a   Clarke, Adrienne Elizabeth ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GOSSYPIUM HIRSUTUM; NICOTIANA TABACUM;

EID: 84867136301     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.203075     Document Type: Article

References (75)

1. Acosta-García G, Vielle-Calzada J-P (2004) A classical arabinogalactan protein is essential for the initiation of female gametogenesis in Arabidopsis. Plant Cell 16: 2614-2628.
2. Albersheim P, Nevins DJ, English PD, Karr A (1967) A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr Res 5: 340-345.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Ben Amar A, Cobanov P, Boonrod K, Krczal G, Bouzid S, Ghorbel A, Reustle GM (2007) Efficient procedure for grapevine embryogenic suspension establishment and plant regeneration: role of conditioned medium for cell proliferation. Plant Cell Rep 26: 1439-1447.
5. Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
6. Bevan M (1984) Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res 12: 8711-8721.
7. Borderies G, le Béchec M, Rossignol M, Lafitte C, Le Deunff E, Beckert M, Dumas C, Elisabeth MR (2004) Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur J Cell Biol 83: 205-212.
8. Borner GHH, Sherrier DJ, Stevens TJ, Arkin IT, Dupree P (2002) Prediction of glycosylphosphatidylinositol-anchored proteins in Arabidopsis: a genomic analysis. Plant Physiol 129: 486-499.
9. Chapman A, Blervacq A-S, Vasseur J, Hilbert J-L (2000) Arabinogalactanproteins in Cichorium somatic embryogenesis: effect of b-glucosyl Yariv reagent and epitope localisation during embryo development. Planta 211: 305-314.
10. Ciucanu I, Kerek F (1984) A simple and rapid method for the permethylation of carbohydrates. Carbohydr Res 131: 209-217 694.
11. Coimbra S, Costa M, Jones B, Mendes MA, Pereira LG (2009) Pollen grain development is compromised in Arabidopsis agp6 agp11 null mutants. J Exp Bot 60: 3133-3142.
12. de Blank C, Mylona P, Yang WC, Katinakis P, Bisseling T, Franssen H (1993) Characterization of the soybean early nodulin cDNA clone GmENOD55. Plant Mol Biol 22: 1167-1171.
13. De Jong AJ, Heidstra R, Spaink HP, Hartog MV, Meijer EA, Hendriks T, Schiavo FL, Terzi M, Bisseling T, Van Kammen A, et al (1993) Rhizobium lipooligosaccharides rescue a carrot somatic embryo mutant. Plant Cell 5: 615-620.
14. de Vries SC, Booij H, Janssens R, Vogels R, Saris L, Lo Schiavo F, Terzi M, van Kammen A (1988) Carrot somatic embryogenesis depends on the phytohormone-controlled presence of correctly glycosylated extracellular proteins. Genes Dev 2: 462-476.
15. Domon J-M, Neutilings G, Roger D, David A, David H (2000) A basic chitinase-like protein secreted by embryogenic tissues of Pinus caribaea acts on arabinogalactan proteins extracted from the same cell lines. J Plant Physiol 156: 33-39.
16. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric methods for the determination of sugars and related substances. Anal Chem 18: 350-356.
17. Dyachok JV, Wiweger M, Kenne L, von Arnold S (2002) Endogenous Nodfactor-like signal molecules promote early somatic embryo development in Norway spruce. Plant Physiol 128: 523-533.
18. Egertsdotter U, von Arnold S (1988) Development of somatic embryos in Norway spruce. J Exp Bot 49: 155-162.
19. Egertsdotter U, von Arnold S (1995) Importance of arabinogalactan proteins for the development of somatic embryos of Norway spruce (Picea abies). Physiol Plant 93: 334-345.
20. Eisenhaber B, Wildpaner M, Schultz CJ, Borner GHH, Dupree P, Eisenhaber F (2003) Glycosylphosphatidylinositol lipid anchoring of plant proteins: sensitive prediction from sequenceand genome-wide studies for Arabidopsis and rice. Plant Physiol 133: 1691-1701.
21. Ellis M, Egelund J, Schultz CJ, Bacic A (2010) Arabinogalactan-proteins: key regulators at the cell surface? Plant Physiol 153: 403-419.
22. Filisetti-Cozzi TMCC, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197: 157-162.
23. Fincher GB, Stone BA, Clarke AE (1993) Arabinogalactan-proteins: structure, biosynthesis and function. Annu Rev Plant Physiol Plant Mol Biol 34: 47-70.
24. Ganjian I, Basile DV (1997) Reductive syntheses of p-aminophenyl-b-Dglucoside and its conversion to b-glucosyl Yariv reagent. Anal Biochem 246: 152-155.
25. Greene EA, Erard M, Dedieu A, Barker DG (1998) MtENOD16 and 20 are members of a family of phytocyanin-related early nodulins. Plant Mol Biol 36: 775-783.
26. Khan JA, Wang Q, Sjölund RD, Schulz A, Thompson GA (2007) An early nodulin-like protein accumulates in the sieve element plasma membrane of Arabidopsis. Plant Physiol 143: 1576-1589.
27. Kim JB, Carpita NC (1992) Changes in esterification of the uronic acid groups of cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol 98: 646-653.
28. Knox JP (2006) Up against the wall: arabinogalactan-protein dynamics at cell surfaces. New Phytol 169: 443-445.
29. Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238: 106-119.
30. Kreuger M, Postma E, Brouwer Y, van Holst G-J (1995) Somatic embryogenesis of Cyclamen persicum in liquid medium. Physiol Plant 94: 605-612.
31. Kreuger M, van Holst G-J (1993) Arabinogalactan proteins are essential in somatic embryogenesis of Daucus carota L. Planta 189: 243-248.
32. Kreuger M, van Holst G-J (1995) Arabinogalactan-protein epitopes in somatic embryogenesis of Daucus carota L. Planta 1995: 135-141.
33. Kyo M, Miyatake H, Mamezuka K, Amagata K (2000) Cloning of cDNA encoding NtEPc, a marker protein for the embryogenic dedifferentiation of immature tobacco pollen grains cultured in vitro. Plant Cell Physiol 41: 129-137.
34. Kyo M, Yamaji N, Yuasa Y, Maeda T, Fukui H (2002) Isolation of cDNAs coding for NtEPb1-b3, marker proteins for pollen dedifferentiation in a tobacco pollen culture system. Plant Sci 163: 1055-1061.
35. Lamport DTA, Kieliszewski MJ, Showalter AM (2006) Salt stress upregulates periplasmic arabinogalactan proteins: using salt stress to analyse AGP function. New Phytol 169: 479-492.
36. Letarte J, Simion E, Miner M, Kasha KJ (2006) Arabinogalactans and arabinogalactan-proteins induce embryogenesis in wheat (Triticum aestivum L.) microspore culture. Plant Cell Rep 24: 691-698.
37. Levitin B, Richter D, Markovich I, Zik M (2008) Arabinogalactan proteins 6 and 11 are required for stamen and pollen function in Arabidopsis. Plant J 56: 351-363.
38. Li YJ, Liu DQ, Tu LL, Zhang XL, Wang L, Zhu LF, Tan JF, Deng FL (2010) Suppression of GhAGP4 gene expression repressed the initiation and elongation of cotton fiber. Plant Cell Rep 29: 193-202.
39. Ma HL, Zhao J (2010) Genome-wide identification, classification, and expression analysis of the arabinogalactan protein gene family in rice (Oryza sativa L.). J Exp Bot 61: 2647-2668.
40. MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus. Plant J 62: 689-703.
41. Mashiguchi K, Asami T, Suzuki Y (2009) Genome-wide identification, structure and expression studies, and mutant collection of 22 early nodulin-like protein genes in Arabidopsis. Biosci Biotechnol Biochem 73: 2452-2459.
42. Mashiguchi K, Yamaguchi I, Suzuki Y (2004) Isolation and identification of glycosylphosphatidylinositol-anchored arabinogalactan proteins and novel b-glucosyl Yariv-reactive proteins from seeds of rice (Oryza sativa). Plant Cell Physiol 45: 1817-1829.
43. McCabe PF, Valentine TA, Forsberg LS, Pennell RI (1997) Soluble signals from cells identified at the cell wall establish a developmental pathway in carrot. Plant Cell 9: 2225-2241.
44. Mort AJ, Lamport DTA (1977) Anhydrous hydrogen fluoride deglycosylates glycoproteins. Anal Biochem 82: 289-309.
45. Motose H, Sugiyama M, Fukuda H (2004) A proteoglycan mediates inductive interaction during plant vascular development. Nature 429: 873-878.
46. Nersissian AM, Immoos C, Hill MG, Hart PJ, Williams G, Herrmann RG, Valentine JS (1998) Uclacyanins, stellacyanins, and plantacyanins are distinct subfamilies of phytocyanins: plant-specific mononuclear blue copper proteins. Protein Sci 7: 1915-1929.
47. Nersissian AM, Shipp EL (2002) Blue copper-binding domains. Adv Protein Chem 60: 271-340.
48. Newman TC, Ohme-Takagi M, Taylor CB, Green PJ (1993) DST sequences, highly conserved among plant SAUR genes, target reporter transcripts for rapid decay in tobacco. Plant Cell 5: 701-714.
49. Nothnagel EA (1997) Proteoglycans and related components in plant cells. Int Rev Cytol 174: 195-291.
50. Paire A, Devaux P, Lafitte C, Dumas C, Matthys-Rochon E (2003) Proteins produced by barley microspores and their derived androgenic structures promote in vitro zygotic maize embryo formation. Plant Cell Tissue Organ Cult 73: 167-176.
51. Reddy PM, Aggarwal RK, Ramos MC, Ladha JK, Brar DS, Kouchi H (1999) Widespread occurrence of the homologues of the early nodulin (ENOD) genes in Oryza species and related grasses. Biochem Biophys Res Commun 258: 148-154.
52. Saare-Surminski K, Preil W, Knox JP, Lieberel R (2000) Arabinogalactan proteins in embryogenic and non-embryogenic callus cultures of Euphorbia pulcherrima. Physiol Plant 108: 180-187.
53. Samaj J, Salaj T, Matúsová R, Salaj J, Takác T, Samajová O, Volkmann D (2008) Arabinogalactan-protein epitope Gal4 is differentially regulated and localized in cell lines of hybrid fir (Abies alba 3 Abies cephalonica) with different embryogenic and regeneration potential. Plant Cell Rep 27: 221-229.
54. Schultz C, Gilson P, Oxley D, Youl J, Bacic A (1998) GPI-anchors on arabinogalactan-proteins: implications for signalling in plants. Trends Plant Sci 3: 426-431.
55. Schultz CJ, Johnson KL, Currie G, Bacic A (2000) The classical arabinogalactan protein gene family of Arabidopsis. Plant Cell 12: 1751-1768.
56. Schultz CJ, Rumsewicz MP, Johnson KL, Jones BJ, Gaspar YM, Bacic A (2002) Using genomic resources to guide research directions: the arabinogalactan protein gene family as a test case. Plant Physiol 129: 1448-1463.
57. Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58: 137-161.
58. Shi H, Kim Y, Guo Y, Stevenson B, Zhu J-K (2003) The Arabidopsis SOS5 locus encodes a putative cell surface adhesion protein and is required for normal cell expansion. Plant Cell 15: 19-32.
59. Shim YS, Pauls KP, Kasha KJ (2009) Transformation of isolated barley (Hordeum vulgare L.) microspores. II. Timing of pretreatment and temperatures relative to results of bombardment. Genome 52: 175-190.
60. Shimizu M, Igasaki T, Yamada M, Yuasa K, Hasegawa J, Kato T, Tsukagoshi H, Nakamura K, Fukuda H, Matsuoka K (2005) Experimental determination of proline hydroxylation and hydroxyproline arabinogalactosylation motifs in secretory proteins. Plant J 42: 877-889.
61. Tan L, Leykam JF, Kieliszewski MJ (2003) Glycosylation motifs that direct arabinogalactan addition to arabinogalactan-proteins. Plant Physiol 132: 1362-1369.
62. Tang X-C, He Y-Q, Wang Y, Sun M-X (2006) The role of arabinogalactan proteins binding to Yariv reagents in the initiation, cell developmental fate, and maintenance of microspore embryogenesis in Brassica napus L. cv. Topas. J Exp Bot 57: 2639-2650.
63. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
64. Toonen MAJ, Schmidt EDL, van Kammen A, de Vries SC (1997) Promotive and inhibitory effects of diverse arabinogalactan proteins on Daucus carota L. somatic embryogenesis. Planta 203: 188-195.
65. Umbeck P, Johnson G, Barton K, Swain W (1987) Genetically transformed cotton (Gossypium hirsutum L) plants. Bio/technology 5: 263-266.
66. van Hengel AJ, Roberts K (2003) AtAGP30, an arabinogalactan-protein in the cell walls of the primary root, plays a role in root regeneration and seed germination. Plant J 36: 256-270.
67. van Hengel AJ, Tadesse Z, Immerzeel P, Schols H, van Kammen A, de Vries SC (2001) N-Acetylglucosamine and glucosamine-containing arabinogalactan proteins control somatic embryogenesis. Plant Physiol 125: 1880-1890.
68. van Hengel AJ, Van Kammen A, De Vries SC (2002) A relationship between seed development, arabinogalactan-proteins (AGPs) and the AGP mediated promotion of somatic embryogenesis. Physiol Plant 114: 637-644.
69. Wu XM, Li FG, Zhang CJ, Liu CL, Zhang XY (2009) Differential gene expression of cotton cultivar CCRI24 during somatic embryogenesis. J Plant Physiol 166: 1275-1283.
70. Xu JF, Tan L, Lamport DTA, Showalter AM, Kieliszewski MJ (2008) The O-Hyp glycosylation code in tobacco and Arabidopsis and a proposed role of Hyp-glycans in secretion. Phytochemistry 69: 1631-1640.
71. Yang J, Sardar HS, McGovern KR, Zhang YZ, Showalter AM (2007) A lysine-rich arabinogalactan protein in Arabidopsis is essential for plant growth and development, including cell division and expansion. Plant J 49: 629-640.
72. Yariv J, Lis H, Katchalski E (1967) Precipitation of arabic acid and some seed polysaccharides by glycosylphenylazo dyes. Biochem J 105: 1C-2C.
73. Yoshizaki M, Furumoto T, Hata S, Shinozaki M, Izui K (2000) Characterization of a novel gene encoding a phytocyanin-related protein in morning glory (Pharbitis nil). Biochem Biophys Res Commun 268: 466-470.
74. Zeng F, Zhang X, Zhu L, Tu L, Guo X, Nie Y (2006) Isolation and characterization of genes associated to cotton somatic embryogenesis by suppression subtractive hybridization and macroarray. Plant Mol Biol 60: 167-183.
75. Zhu Y, Pettolino F, Mau S-L, Bacic A (2005) Characterization of cell wall polysaccharides from the medicinal plant Panax notoginseng. Phytochemistry 66: 1067-1076.