BnPME is progressively induced after microspore reprogramming to embryogenesis, correlating with pectin de-esterification and cell differentiation in Brassica napus

BMC Plant Biology

Volumn 16, Issue 1, 2016, Pages

  Solís, María Teresa ^a   Berenguer, Eduardo ^a   Risueño, María C ^a   Testillano, Pilar S ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Cell reprogramming; Cell wall remodeling; Differentiation; Gametophytic development; Microspore embryogenesis; Pectin esterification; Pectin methylesterase; Pollen; Proliferation; Totipotency

Indexed keywords

ESTERASE; PECTIN; PLANT PROTEIN;

CELL DIFFERENTIATION; CYTOLOGY; EMBRYOLOGY; ENZYMOLOGY; ESTERIFICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RAPESEED;

BRASSICA NAPUS; CELL DIFFERENTIATION; ESTERASES; ESTERIFICATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; PECTINS; PLANT PROTEINS;

EID: 84991728770     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/s12870-016-0863-8     Document Type: Article

References (69)

1. Knox JP. Revealing the structural and functional diversity of plant cell walls. Curr Op Plant Biol. 2008;11:308-13.
2. Pelloux J, Rusterucci C, Mellerowicz EJ. New insights into pectin methylesterase structure and function. Trends Plant Sci. 2007;12:267-77.
3. Willats WGT, Orfila C, Limberg G, Buchholt HC, Van Alebeek G, Voragen AGJ, Marcus SE, Christensen T, Mikkelsen JD, Murray BS, et al. Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls-Implications for pectin methyl esterase action, matrix properties, and cell adhesion. J Biol Chem. 2001;276:19404-13.
4. Tieman DM, Handa AK. Reduction in pectin methylesterase activity modifies tissue integrity and cation levels in ripening tomato (Lycopersicon-Esculentum mill) fruits. Plant Phys. 1994;106:429-36.
5. Wen FS, Zhu YM, Hawes MC. Effect of pectin methylesterase gene expression on pea root development. Plant Cell. 1999;11:1129-40.
6. Micheli F, Sundberg B, Goldberg R, Richard L. Radial distribution pattern of pectin methylesterases across the cambial region of hybrid aspen at activity and dormancy. Plant Phys. 2000;124:191-9.
7. Micheli F. Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends Plant Sci. 2001;6:414-9.
8. Bosch M, Cheung AY, Hepler PK. Pectin methylesterase, a regulator of pollen tube growth. Plant Phys. 2005;138:1334-46.
9. Tian G-W, Chen M-H, Zaltsman A, Citovsky V. Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol. 2006;294:83-91.
10. Pilling J, Willmitzer L, Fisahn J. Expression of a Petunia inflata pectin methyl esterase in Solanum tuberosum L. enhances stem elongation and modifies cation distribution. Planta. 2000;210:391-9.
11. Pilling J, Willmitzer L, Bucking H, Fisahn J. Inhibition of a ubiquitously expressed pectin methyl esterase in Solanum tuberosum L. affects plant growth, leaf growth polarity, and ion partitioning. Planta. 2004;219:32-40.
12. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D. VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell. 2005;17: 584-96.
13. Bosch M, Hepler PK. Silencing of the tobacco pollen pectin methylesterase NtPPME1 results in retarded in vivo pollen tube growth. Planta. 2006;223: 736-45.
14. Francis KE, Lam SY, Copenhaver GP. Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Phys. 2006; 142:1004-13.
15. Maluszynski M, Kasha K, Forster B, Szarejko I. Doubled haploid production in crop plants: a manual. Kluwer: Dordrecht; 2003.
16. Bárány I, González-Melendi P, Fadón B, Mityko J, Risueño MC, Testillano PS. Microspore-derived embryogenesis in pepper (Capsicum annuum L.): subcellular rearrangements through development. Biol Cell. 2005;97:709-22.
17. Prem D, Solís MT, Bárány I, Rodríguez-Sánz H, Risueño MC, Testillano PS. A new microspore embryogenesis system under low temperature which mimics zygotic embryogenesis initials, expresses auxin and efficiently regenerates doubled-haploid plants in Brassica napus. BMC Plant Biol. 2012;12:127.
18. Testillano PS, Coronado MJ, Seguí JM, Domenech J, González-Melendi P, Raska I, Risueño MC. Defined nuclear changes accompany the reprogramming of the microspore to embryogenesis. J Struct Biol. 2000;129:223-32.
19. Testillano PS, Ramírez C, Domenech J, Coronado MJ, Vergne P, Matthys-Rochon E, Risueño MC. Young microspore-derived maize embryos show two domains with defined features also present in zygotic embryogenesis. Int J Dev Biol. 2002;46:1035-47.
20. Seguí-Simarro J, Testillano P, Jouannic S, Henry Y, Risueño M. Mitogenactivated protein kinases are developmentally regulated during stressinduced microspore embryogenesis in Brassica napus L. Histochem Cell Biol. 2005;123:541-51.
21. El-Tantawy AA, Solís MT, Risueño MC, Testillano PS. Changes in DNA methylation levels and nuclear distribution patterns after microspore reprogramming to embryogenesis in barley. Cytogenet Genome Res. 2014; 143:200-208.
22. Coronado MJ, González-Melendi P, Seguí JM, Ramírez C, Barany I, Testillano PS, Risueño MC. MAPKs entry into the nucleus at specific interchromatin domains in plant differentiation and proliferation processes. J Struct Biol. 2002;140:200-13.
23. Testillano PS, Risueño MC. Tracking gene and protein expression during microspore embryogenesis by confocal laser scanning microscopy. In: Touraev A, Forster BP, Mohan Jain S, editors. Advances in Haploid Production in Higher Plants. UK: Springer Science and Bussines Media B.V;. 2009. p. 339-47.
24. Malinowski R, Filipecki M. The role of cell wall in plant embryogenesis. Cell Mol Biol Letters. 2002;7:1137-51.
25. Fortes AM, Testillano PS, Risueño MD, Pais MS. Studies on callose and cutin during the expression of competence and determination for organogenic nodule formation from internodes of Humulus lupulus var. Nugget Physiologia Plantarum. 2002;116:113-20.
26. Solís MT, Pintos B, Prado MJ, Bueno MA, Raska I, Risueño MC, Testillano PS. Early markers of in vitro microspore reprogramming to embryogenesis in olive (Olea europaea L.). Plant Sci. 2008;174:597-605.
27. Bárány I, Fadón B, Risueño MC, Testillano PS. Cell wall components and pectin esterification levels as markers of proliferation and differentiation events during pollen development and pollen embryogenesis in Capsicum annuum L. J Exp Bot. 2010;61:1159-75.
28. El-Tantawy AA, Solís MT, Da Costa ML, Coimbra S, Risueño MC, Testillano PS. Arabinogalactan protein profiles and distribution patterns during microspore embryogenesis and pollen development in Brassica napus. Plant Reprod. 2013;26:231-43.
29. Bárány I, Fadón B, Risueño MC, Testillano PS. Microspore reprogramming to embryogenesis induces changes in cell wall and starch accumulation dynamics associated with proliferation and differentiation events. Plant Signal Behav. 2010;5:341-5.
30. Ramírez C, Testillano PS, Pintos B, Moreno-Risueño MA, Bueno MA, Risueño MC. Changes in pectins and MAPKs related to cell development during early microspore embryogenesis in Quercus suber L. Eur J Cell Biol. 2004; 83:213-25.
31. Coutinho PM, Starn M, Blanc E, Henrissat B. Why are there so many carbohydrate-active enzyme-related genes in plants? Trends Plant Sci. 2003;8:563-5.
32. Gómez MD, Renau-Morata B, Roque E, Polaina J, Beltran JP, Cañas LA. PsPMEP, a pollen-specific pectin methylesterase of pea (Pisum sativum L.). Plant Reprod. 2013;26:245-54.
33. Rexova-Benkova L, Markovic O. Pectic enzymes. Adv Carbohydrate Chem Biochem. 1976;33:323-85.
34. Jolie RP, Duvetter T, Van Loey AM, Hendrickx ME. Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydrate Res. 2010;345:2583-95.
35. Xu C, Zhao L, Pan X, Samaj J. Developmental localization and methylesterification of pectin epitopes during somatic embryogenesis of banana (Musa spp. AAA). PLoS ONE. 2011;6:e22992.
36. Christgau S, Kofod LV, Halkier T, Andersen LN, Hockauf M, Dorreich K, Dalboge H, Kauppinen S. Pectin methyl esterase from Aspergillus aculeatus: expression cloning in yeast and characterization of the recombinant enzyme. Biochem J. 1996;319:705-12.
37. Rodríguez-Sanz H, Manzanera JA, Solís MT, Gómez-Garay A, Pintos B, Risueño MC, Testillano PS. Early markers are present in both embryogenesis pathways from microspores and immature zygotic embryos in cork oak, Quercus suber L. BMC Plant Biol. 2014;14:224.
38. Senechal F, Wattier C, Rusterucci C, Pelloux J. Homogalacturonan-modifying enzymes: structure, expression, and roles in plants. J Exp Bot. 2014;65:5125-60.
39. Zhang GY, Feng J, Wu J, Wang XW. BoPMEI1, a pollen-specific pectin methylesterase inhibitor, has an essential role in pollen tube growth. Planta. 2010;231:1323-34.
40. Kang Y, Nasrallah J. Use of genetically ablated stigmas for the isolation of genes expressed specifically in the stigma epidermis. Sex Plant Rep. 2001; 14:85-94.
41. Knox JP, Linstead PJ, King J, Cooper C, Roberts K. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta. 1990;181:512-21.
42. Clausen MH, Willats WG, Knox JP. Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Res. 2003;338:1797-800.
43. Goldberg R, Morvan C, Roland JC. Composition, properties and localization of pectins in young and mature cells of the mung bean hypocotyl. Plant Cell Phys. 1986;27:417-29.
44. Dolan L, Linstead P, Roberts K. Developmental regulation of pectic polysaccharides in the root meristem of Arabidopsis. J Exp Bot. 1997;48:713-20.
45. Hasegawa Y, Nakamura S, Uheda E, Nakamura N. Immunolocalization and possible roles of pectins during pollen growth and callose plug formation in angiosperms. Grana. 2000;39:46-55.
46. González-Melendi P, Testillano PS, Ahmadian P, Fadón B, Vicente O, Risueño MC. In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum. Protoplasma. 1995;187:60-71.
47. Testillano PS, González-Melendi P, Coronado MJ, Seguí-Simarro JM, Moreno-Risueño MA, Risueño MC. Differentiating plant cells switched to proliferation remodel the functional organization of nuclear domains. Cytogen Genome Res. 2005;109:166-74.
48. Solís MT, Rodríguez-Serrano M, Meijón M, Cañal MJ, Cifuentes A, Risueño MC, Testillano PS. DNA methylation dynamics and MET1a-like gene expression changes during stress-induced pollen reprogramming to embryogenesis. J Exp Bot. 2012;63:6431-44.
49. Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, Pereira LG, Coimbra S. Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol. 2013;13:7.
50. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2 (-Delta Delta C (T)) method. Methods. 2001;25:402-8.
51. Batoko H, Zheng HQ, Hawes C, Moore I. A rab1 GTPase is required for transport between the endoplasmic reticulum and golgi apparatus and for normal golgi movement in plants. Plant Cell. 2000;12:2201-18.
52. Bueno MA, Gomez A, Sepulveda F, Segui JM, Testillano PS, Manzanera JA, Risueno MC. Microspore-derived embryos from Quercus suber anthers mimic zygotic embryos and maintain haploidy in long-term anther culture. J Plant Physiol. 2003;160:953-60.
53. Guglielmino N, Liberman M, Catesson AM, Mareck A, Prat R, Mutaftschiev S, Goldberg R. Pectin methylesterases from poplar cambium and inner bark: Localization, properties and seasonal changes. Planta. 1997;202:70-5.
54. Parre E, Geitmann A. Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta. 2005;220:582-92.
55. Louvet R, Cavel E, Gutierrez L, Guenin S, Roger D, Gillet F, Guerineau F, Pelloux J. Comprehensive expression profiling of the pectin methylesterase gene family during silique development in Arabidopsis thaliana. Planta. 2006;224:782-91.
56. Wolf S, Mouille G, Pelloux J. Homogalacturonan Methyl-Esterification and Plant Development. Mol Plant. 2009;2:851-60.
57. Levesque-Tremblay G, Muller K, Mansfield SD, Haughn GW. HIGHLY METHYL ESTERIFIED SEEDS is a pectin methyl esterase involved in embryo development. Plant Phys. 2015;167:725-37.
58. Braybrook SA, Peaucelle A. Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS ONE. 2013;8:e57813.
59. Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Hofte H. Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Current Biol. 2011;21:1720-6.
60. Moller B, Weijers D. Auxin control of embryo patterning. Cold Spring Harbor Perspect Biol. 2009;1:a001545.
61. Rodriguez-Sanz H, Solis MT, Lopez MF, Gomez-Cadenas A, Risueno MC, Testillano PS. Auxin Biosynthesis, Accumulation, Action and Transport are Involved in Stress-Induced Microspore Embryogenesis Initiation and Progression in Brassica napus. Plant Cell Phys. 2015;56:1401-17.
62. Quentin M, Jauneau A, Morvan O, Morvan C. Immunolocalization of pectin methylestareses in the hypocotyl tissues of flax. Plant Phys Biochem. 1997; 35:475-82.
63. Rodriguez-Sanz H, Moreno-Romero J, Solis MT, Kohler C, Risueno MC, Testillano PS. Changes in Histone Methylation and Acetylation during Microspore Reprogramming to Embryogenesis Occur Concomitantly with BnHKMT and BnHAT Expression and Are Associated with Cell Totipotency, Proliferation, and Differentiation in Brassica napus. Cytogen Genome Res. 2014;143:209-18.
64. Peaucelle A, Louvet R, Johansen JN, Hofte H, Laufs P, Pelloux J, Mouille G. Arabidopsis phyllotaxis is controlled by the methyl-esterification status of cell-wall pectins. Current Biol. 2008;18:1943-8.
65. Ramírez C, Chiancone B, Testillano PS, García-Fojeda B, Germana MA, Risueño MC. First embryogenic stages of Citrus microspore-derived embryos. Acta Biol Cracov Ser Bot. 2003;45:53-8.
66. Willats WGT, McCartney L, Mackie W, Knox JP. Pectin: cell biology and prospects for functional analysis. Plant Mol Biol. 2001;47:9-27.
67. Li YQ, Mareck A, Faleri C, Moscatelli A, Liu Q, Cresti M. Detection and localization of pectin methylesterase isoforms in pollen tubes of Nicotiana tabacum L. Planta. 2002;214:734-40.
68. Bosch M, Hepler PK. Pectin methylesterases and pectin dynamics in pollen tubes. Plant Cell. 2005;17:3219-26.
69. Leroux C, Bouton S, Kiefer-Meyer MC, Fabrice TN, Mareck A, Guenin S, Fournet F, Ringli C, Pelloux J, Driouich A, et al. PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant Phys. 2015;167: 367-80.