Sulfinylated azadecalins act as functional mimics of a pollen germination stimulant in Arabidopsis pistils

Plant Journal

Volumn 68, Issue 5, 2011, Pages 800-815

  Qin, Yuan ^a,e   Wysocki, Ronald J ^b   Somogyi, Arpad ^b   Feinstein, Yelena ^a   Franco, Jessica Y ^a   Tsukamoto, Tatsuya ^a   Dunatunga, Damayanthi ^a   Levy, Clara ^c   Smith, Steven ^a   Simpson, Robert ^d,f   Gang, David ^a   Johnson, Mark A ^a   Palanivelu, Ravishankar ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

^c BROWN UNIVERSITY   (United States)

^d PIMA COMMUNITY COLLEGE   (United States)

^e INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

^f WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

chemical biology; functional mimic; germination; pistil; pollen; stimulant

Indexed keywords

CHEMICAL BIOLOGY; FUNCTIONAL MIMICS; GERMINATION; PISTIL; POLLEN; STIMULANT;

CULTIVATION; ELECTROSPRAY IONIZATION; IONS;

PLANTS (BOTANY);

ARABIDOPSIS PROTEIN; PLANT EXTRACT; QUINOLINE DERIVATIVE; SULFOXIDE;

ARABIDOPSIS; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECT; ELECTROSPRAY MASS SPECTROMETRY; FLOWER; GERMINATION; GROWTH, DEVELOPMENT AND AGING; INFRARED SPECTROSCOPY; METHODOLOGY; POLLEN; SPECIES DIFFERENCE; TANDEM MASS SPECTROMETRY; TIME;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GERMINATION; MOLECULAR STRUCTURE; PLANT EXTRACTS; POLLEN; QUINOLINES; SPECIES SPECIFICITY; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; SULFOXIDES; TANDEM MASS SPECTROMETRY; TIME FACTORS;

ARABIDOPSIS; BRASSICACEAE; NICOTIANA TABACUM; SISYMBRIUM IRIO;

EID: 82355175302     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2011.04729.x     Document Type: Article

References (49)

1. Beilstein, M.A., Al-Shehbaz, I.A., and, Kellogg, E.A., (2006) Brassicaceae phylogeny and trichome evolution. Am. J. Bot. 93, 607-619.
2. Beilstein, M.A., Nagalingum, N.S., Clements, M.D., Manchester, S.R., and, Mathews, S., (2010) Dated molecular phylogenies indicate a Miocene origin for Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 107, 18724-18728.
3. Boavida, L.C., and, McCormick, S., (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52, 570-582. (Pubitemid 47621873)
4. Bou Daher, F., Chebli, Y., and, Geitmann, A., (2008) Optimization of conditions for germination of cold-stored Arabidopsis thaliana pollen. Plant Cell Rep. 28, 347-357.
5. Burbulis, I.E., Iacobucci, M., and, Shirley, B.W., (1996) A null mutation in the first enzyme of flavonoid biosynthesis does not affect male fertility in Arabidopsis. Plant Cell, 8, 1013-1025. (Pubitemid 26324296)
6. Chapman, L.A., and, Goring, D.R., (2010) Pollen-pistil interactions regulating successful fertilization in the Brassicaceae. J. Exp. Bot. 61, 1987-1999.
7. Chemla, F., and, Ferreira, F., (2004) Diastereoselective synthesis of trans-ethynyl N-tert-butanesulfinylaziridines. Synlett, 6, 983-986.
8. Chen, S., Zhao, Y., and, Wang, J., (2006) Preparation of cyclic N-tert-butylsulfonyl enamines by Rh(II)-mediated ring expansion of α-diazoesters. Synthesis, 10, 1705-1710. (Pubitemid 43805980)
9. Edlund, A.F., Swanson, R., and, Preuss, D., (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell, 16 (Suppl), S84-S97. (Pubitemid 38774219)
10. Elleman, C.J., Franklin-Tong, V., and, Dickinson, H.G., (1992) Pollination in species with dry stigmas: the nature of the early stigmatic response and the pathway taken by pollen tubes. New Phytol. 121, 413-424. (Pubitemid 23397526)
11. Gu, Y., Wang, Z., and, Yang, Z., (2004) ROP/RAC GTPase: an old new master regulator for plant signaling. Curr. Opin. Plant Biol. 7, 527-536. (Pubitemid 39175150)
12. Han, H.Y., Shan, S., Zhang, X., Wang, N.L., Lu, X.P., and, Yao, X.S., (2007) Down-regulation of prostate specific antigen in LNCaP cells by flavonoids from the pollen of Brassica napus L. Phytomedicine, 14, 338-343. (Pubitemid 46654788)
13. 2+-channel blocker, nifedipine. Ann. Bot. 69, 395-403.
14. Heslop-Harrison, Y., and, Heslop-Harrison, J., (1992b) Germination of monocolpate angiosperm pollen: evolution of the actin cytoskeleton and wall during hydration, activation and tube emergence. Ann. Bot. 69, 385-394.
15. Hicks, G.R., Rojo, E., Hong, S., Carter, D.G., and, Raikhel, N.V., (2004) Geminating pollen has tubular vacuoles, displays highly dynamic vacuole biogenesis, and requires VACUOLESS1 for proper function. Plant Physiol. 134, 1227-1239. (Pubitemid 38398270)
16. Higashiyama, T., and, Hamamura, Y., (2008) Gametophytic pollen tube guidance. Sex. Plant Reprod. 21, 17-26.
17. Holdaway-Clarke, T.L., and, Hepler, P.K., (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol. 159, 539-563. (Pubitemid 37024061)
18. 2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol. 136, 3562-3571. (Pubitemid 41075795)
19. Jackson, C.L., and, Hartwell, L.H., (1990) Courtship in S. cerevisiae: both cell types choose mating partners by responding to the strongest pheromone signal. Cell, 63, 1039-1051. (Pubitemid 120034945)
20. Johnson, S.A., and, McCormick, S., (2001) Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol. 126, 685-695. (Pubitemid 32566621)
21. Johnson, M.A., von Besser, K., Zhou, Q., Smith, E., Aux, G., Patton, D., Levin, J.Z., and, Preuss, D., (2004) Arabidopsis hapless mutations define essential gametophytic functions. Genetics, 168, 971-982. (Pubitemid 39491472)
22. Johnson-Brousseau, S.A., and, McCormick, S., (2004) A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant J. 39, 761-775. (Pubitemid 39218783)
23. Kim, Y., Song, K., and, Cheong, H., (1996) Effects of flavonoids on pollen tube growth in Arabidopsis thaliana. J. Plant. Biol. 39, 273-278.
24. Kim, S., Mollet, J.C., Dong, J., Zhang, K., Park, S.Y., and, Lord, E.M., (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc. Natl Acad. Sci. USA, 100, 16125-16130. (Pubitemid 38021125)
25. Lalanne, E., and, Twell, D., (2002) Genetic control of male germ unit organization in Arabidopsis. Plant Physiol. 129, 865-875. (Pubitemid 34689166)
26. Li, H., Lin, Y., Heath, R.M., Zhu, M.X., and, Yang, Z., (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell, 11, 1731-1742.
27. Li, S., Gu, Y., Yan, A., Lord, E., and, Yang, Z.-B., (2008) RIP1 (ROP Interactive Partner 1)/ICR1 Marks pollen germination sites and may act in the ROP1 pathway in the control of polarized pollen growth. Molecular Plant, 1, 1021-1035.
28. Malhõ, R., Hwang, J.-U., and, Yang, Z., (2006) Small GTPases and spatiotemporal regulation of pollen tube growth. In The Pollen Tube. Heidelberg: Springer Berlin, pp. 95-116.
29. Mayfield, J.A., and, Preuss, D., (2000) Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat. Cell Biol. 2, 128-130.
30. Mo, Y., Nagel, C., and, Taylor, L.P., (1992) Biochemical complementation of chalcone synthase mutants defines a role for flavonols in functional pollen. Proc. Natl Acad. Sci. USA, 89, 7213-7217.
31. Okuda, S., Tsutsui, H., Shiina, K., et al. (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature, 458, 357-361.
32. Palanivelu, R., and, Johnson, M.A., (2010) Functional genomics of pollen tube-pistil interactions in Arabidopsis. Biochem. Soc. Trans. 38, 593-597.
33. Palanivelu, R., and, Preuss, D., (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol. 6, 7.
34. Piggott, A.M., and, Karuso, P., (2007) Hydrolysis rates of alkyl and aryl sulfinamides: evidence of general acid catalysis. Tetrahedron Lett. 48, 7452-7455. (Pubitemid 47418914)
35. Pollak, R.E., Hansen, K., Astwood, J.D., and, Taylor, L.R., (1995) Conditional male fertility in maize. Sex. Plant Reprod. 8, 231-241.
36. Qin, Y., Leydon, A.R., Manziello, A., Pandey, R., Mount, D., Denic, S., Vasic, B., Johnson, M.A., and, Palanivelu, R., (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet. 5, e1000621.
37. Raftery, M., and, Geczy, C., (2002) Electrospray low energy CID and MALDI PSD fragmentations of protonated sulfinamide cross-linked peptides. J. Am. Soc. Mass Spectrom. 13, 709-718. (Pubitemid 36876024)
38. Sanchez-Camacho, C., and, Bovolenta, P., (2009) Emerging mechanisms in morphogen-mediated axon guidance. Bioessays, 31, 1013-1025.
39. Shapiro, S.S., and, Wilk, M.B., (1965) An analysis of variance for normality (complete samples). Biometrika, 52, 591-611.
40. Silverstein, R.M., Bassler, G.C., and, Morrill, T.C., (1991) Spectrometric Identification of Organic Compounds, 5th edn. New York: Wiley.
41. Smyth, D.R., Bowman, J.L., and, Meyerowitz, E.M., (1990) Early flower development in Arabidopsis. Plant Cell, 2, 755-767. (Pubitemid 120015483)
42. Sousa, E., Kost, B., and, Malh, R., (2008) Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. Plant Cell, 20, 3050-3064.
43. Taylor, L.P., and, Grotewold, E., (2005) Flavonoids as developmental regulators. Curr. Opin. Plant Biol. 8, 317-323. (Pubitemid 40599985)
44. Tsukamoto, Y., and, Matsubara, S., (1967) Studies on germination of chrysanthemum pollen II. Occurence of a germination-promoting substance. Plant Cell Physiol. 9, 237-245.
45. Tsukamoto, T., Qin, Y., Huang, Y., Dunatunga, D., and, Palanivelu, R., (2010) A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development. Plant J. 62, 571-588.
46. Wengier, D.L., Mazzella, M.A., Salem, T.M., McCormick, S., and, Muschietti, J.P., (2010) STIL, a peculiar molecule from styles, specifically dephosphorylates the pollen receptor kinase LePRK2 and stimulates pollen tube growth in vitro. BMC Plant Biol. 10, 33.
47. Ylstra, B., Touraev, A., Moreno, R.M., Stoger, E., van Tunen, A.J., Vicente, O., Mol, J.N., and, Heberle-Bors, E., (1992) Flavonols stimulate development, germination, and tube growth of tobacco pollen. Plant Physiol. 100, 902-907.
48. Ylstra, B., Muskens, M., and, Van Tunen, A.J., (1996) Flavonols are not essential for fertilization in Arabidopsis thaliana. Plant Mol. Biol. 32, 1155-1158. (Pubitemid 27049913)
49. Zinkl, G.M., Zwiebel, B.I., Grier, D.G., and, Preuss, D., (1999) Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development, 126, 5431-5440. (Pubitemid 30015935)