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. 2004 Apr 9;16(Suppl):S84–S97. doi: 10.1105/tpc.015800

Pollen and stigma structure and function: the role of diversity in pollination.

Anna F Edlund 1, Robert Swanson 1, Daphne Preuss 1
PMCID: PMC2643401  PMID: 15075396

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Selected References

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  1. Alvarez J., Smyth D. R. CRABS CLAW and SPATULA, two Arabidopsis genes that control carpel development in parallel with AGAMOUS. Development. 1999 Jun;126(11):2377–2386. doi: 10.1242/dev.126.11.2377. [DOI] [PubMed] [Google Scholar]
  2. Bih F. Y., Wu S. S., Ratnayake C., Walling L. L., Nothnagel E. A., Huang A. H. The predominant protein on the surface of maize pollen is an endoxylanase synthesized by a tapetum mRNA with a long 5' leader. J Biol Chem. 1999 Aug 6;274(32):22884–22894. doi: 10.1074/jbc.274.32.22884. [DOI] [PubMed] [Google Scholar]
  3. Clark G. B., Turnwald S., Tirlapur U. K., Haas C. J., von der Mark K., Roux S. J., Scheuerlein R. Polar distribution of annexin-like proteins during phytochrome-mediated initiation and growth of rhizoids in the ferns Dryopteris and Anemia. Planta. 1995;197(2):376–384. doi: 10.1007/BF00202660. [DOI] [PubMed] [Google Scholar]
  4. Copenhaver G. P., Keith K. C., Preuss D. Tetrad analysis in higher plants. A budding technology. Plant Physiol. 2000 Sep;124(1):7–16. doi: 10.1104/pp.124.1.7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Copenhaver Gregory P. Using Arabidopsis to understand centromere function: progress and prospects. Chromosome Res. 2003;11(3):255–262. doi: 10.1023/a:1022887926807. [DOI] [PubMed] [Google Scholar]
  6. Dixit R., Rizzo C., Nasrallah M., Nasrallah J. The brassica MIP-MOD gene encodes a functional water channel that is expressed in the stigma epidermis. Plant Mol Biol. 2001 Jan;45(1):51–62. doi: 10.1023/a:1006428007826. [DOI] [PubMed] [Google Scholar]
  7. Doughty J., Hedderson F., McCubbin A., Dickinson H. Interaction between a coating-borne peptide of the Brassica pollen grain and stigmatic S (self-incompatibility)-locus-specific glycoproteins. Proc Natl Acad Sci U S A. 1993 Jan 15;90(2):467–471. doi: 10.1073/pnas.90.2.467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Elleman C. J., Dickinson H. G. Pollen-stigma interactions in Brassica. IV. Structural reorganization in the pollen grains during hydration. J Cell Sci. 1986 Feb;80:141–157. doi: 10.1242/jcs.80.1.141. [DOI] [PubMed] [Google Scholar]
  9. Fiebig Aretha, Kimport Rebecca, Preuss Daphne. Comparisons of pollen coat genes across Brassicaceae species reveal rapid evolution by repeat expansion and diversification. Proc Natl Acad Sci U S A. 2004 Feb 17;101(9):3286–3291. doi: 10.1073/pnas.0305448101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goldman M. H., Goldberg R. B., Mariani C. Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J. 1994 Jul 1;13(13):2976–2984. doi: 10.1002/j.1460-2075.1994.tb06596.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grini P. E., Schnittger A., Schwarz H., Zimmermann I., Schwab B., Jürgens G., Hülskamp M. Isolation of ethyl methanesulfonate-induced gametophytic mutants in Arabidopsis thaliana by a segregation distortion assay using the multimarker chromosome 1. Genetics. 1999 Feb;151(2):849–863. doi: 10.1093/genetics/151.2.849. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gu Ying, Vernoud Vanessa, Fu Ying, Yang Zhenbiao. ROP GTPase regulation of pollen tube growth through the dynamics of tip-localized F-actin. J Exp Bot. 2003 Jan;54(380):93–101. doi: 10.1093/jxb/erg035. [DOI] [PubMed] [Google Scholar]
  13. Hall Anne E., Fiebig Aretha, Preuss Daphne. Beyond the Arabidopsis genome: opportunities for comparative genomics. Plant Physiol. 2002 Aug;129(4):1439–1447. doi: 10.1104/pp.004051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heseltine L., Webster J. M., Taylor R. Adenosine effects upon insulin action on lipolysis and glucose transport in human adipocytes. Mol Cell Biochem. 1995 Mar 23;144(2):147–151. doi: 10.1007/BF00944394. [DOI] [PubMed] [Google Scholar]
  15. Heslop-Harrison J., Heslop-Harrison Y. Germination of stress-tolerant Eucalyptus pollen. J Cell Sci. 1985 Feb;73:135–157. doi: 10.1242/jcs.73.1.135. [DOI] [PubMed] [Google Scholar]
  16. Heslop-Harrison J. The physiology of the pollen grain surface. Proc R Soc Lond B Biol Sci. 1975 Aug 19;190(1100):275–299. doi: 10.1098/rspb.1975.0093. [DOI] [PubMed] [Google Scholar]
  17. Heslop-Harrison J. Wall pattern formation in angiosperm microsporogenesis. Symp Soc Exp Biol. 1971;25:277–300. [PubMed] [Google Scholar]
  18. Hopkins C. Y., Jevans A. W., Boch R. Occurrence of octadeca-trans-2,cis-9,cis-12-trienoic acid in pollen attractive to the honey bee. Can J Biochem. 1969 Apr;47(4):433–436. doi: 10.1139/o69-067. [DOI] [PubMed] [Google Scholar]
  19. Howlett B. J., Knox R. B., Heslop-Harrison J. Pollen-wall proteins: release of the allergen Antigen E from intine and exine sites in pollen grains of ragweed and Cosmos. J Cell Sci. 1973 Sep;13(2):603–619. doi: 10.1242/jcs.13.2.603. [DOI] [PubMed] [Google Scholar]
  20. Hulskamp M., Parekh N. S., Grini P., Schneitz K., Zimmermann I., Lolle S. J., Pruitt R. E. The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev Biol. 1997 Jul 1;187(1):114–124. doi: 10.1006/dbio.1997.8554. [DOI] [PubMed] [Google Scholar]
  21. Hülskamp M., Kopczak S. D., Horejsi T. F., Kihl B. K., Pruitt R. E. Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J. 1995 Nov;8(5):703–714. doi: 10.1046/j.1365-313x.1995.08050703.x. [DOI] [PubMed] [Google Scholar]
  22. Jackson R. C., Skvarla J. J., Chissoe W. F. A unique pollen wall mutation in the family Compositae: ultrastructure and genetics. Am J Bot. 2000 Nov;87(11):1571–1577. [PubMed] [Google Scholar]
  23. Johnson Mark A., Preuss Daphne. Plotting a course: multiple signals guide pollen tubes to their targets. Dev Cell. 2002 Mar;2(3):273–281. doi: 10.1016/s1534-5807(02)00130-2. [DOI] [PubMed] [Google Scholar]
  24. Johnson S. A., McCormick S. Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis gametophytic mutant. Plant Physiol. 2001 Jun;126(2):685–695. doi: 10.1104/pp.126.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Kandasamy M. K., Thorsness M. K., Rundle S. J., Goldberg M. L., Nasrallah J. B., Nasrallah M. E. Ablation of Papillar Cell Function in Brassica Flowers Results in the Loss of Stigma Receptivity to Pollination. Plant Cell. 1993 Mar;5(3):263–275. doi: 10.1105/tpc.5.3.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kang B. H., Busse J. S., Dickey C., Rancour D. M., Bednarek S. Y. The arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiol. 2001 May;126(1):47–68. doi: 10.1104/pp.126.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Kang Byung-Ho, Busse James S., Bednarek Sebastian Y. Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell. 2003 Apr;15(4):899–913. doi: 10.1105/tpc.009670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Kao Teh-hui, Tsukamoto Tatsuya. The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell. 2004 Mar 9;16 (Suppl):S72–S83. doi: 10.1105/tpc.016154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Knox R. B., Heslop-Harrison J. Pollen-wall proteins: localization and enzymic activity. J Cell Sci. 1970 Jan;6(1):1–27. doi: 10.1242/jcs.6.1.1a. [DOI] [PubMed] [Google Scholar]
  30. Kost B., Lemichez E., Spielhofer P., Hong Y., Tolias K., Carpenter C., Chua N. H. Rac homologues and compartmentalized phosphatidylinositol 4, 5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol. 1999 Apr 19;145(2):317–330. doi: 10.1083/jcb.145.2.317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lalanne Eric, Twell David. Genetic control of male germ unit organization in Arabidopsis. Plant Physiol. 2002 Jun;129(2):865–875. doi: 10.1104/pp.003301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lalonde B. A., Nasrallah M. E., Dwyer K. G., Chen C. H., Barlow B., Nasrallah J. B. A highly conserved Brassica gene with homology to the S-locus-specific glycoprotein structural gene. Plant Cell. 1989 Feb;1(2):249–258. doi: 10.1105/tpc.1.2.249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Li H., Lin Y., Heath R. M., Zhu M. X., Yang Z. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell. 1999 Sep;11(9):1731–1742. doi: 10.1105/tpc.11.9.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lolle S. J., Berlyn G. P., Engstrom E. M., Krolikowski K. A., Reiter W. D., Pruitt R. E. Developmental regulation of cell interactions in the Arabidopsis fiddlehead-1 mutant: a role for the epidermal cell wall and cuticle. Dev Biol. 1997 Sep 15;189(2):311–321. doi: 10.1006/dbio.1997.8671. [DOI] [PubMed] [Google Scholar]
  35. Lolle S. J., Cheung A. Y. Promiscuous germination and growth of wildtype pollen from Arabidopsis and related species on the shoot of the Arabidopsis mutant, fiddlehead. Dev Biol. 1993 Jan;155(1):250–258. doi: 10.1006/dbio.1993.1022. [DOI] [PubMed] [Google Scholar]
  36. Lolle S. J., Hsu W., Pruitt R. E. Genetic analysis of organ fusion in Arabidopsis thaliana. Genetics. 1998 Jun;149(2):607–619. doi: 10.1093/genetics/149.2.607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Lord E. M. Adhesion and guidance in compatible pollination. J Exp Bot. 2003 Jan;54(380):47–54. doi: 10.1093/jxb/erg015. [DOI] [PubMed] [Google Scholar]
  38. Lord Elizabeth M., Russell Scott D. The mechanisms of pollination and fertilization in plants. Annu Rev Cell Dev Biol. 2002 Apr 2;18:81–105. doi: 10.1146/annurev.cellbio.18.012502.083438. [DOI] [PubMed] [Google Scholar]
  39. Lush WM, Grieser F, Wolters-Arts M. Directional guidance of nicotiana alata pollen tubes in vitro and on the stigma . Plant Physiol. 1998 Nov;118(3):733–741. doi: 10.1104/pp.118.3.733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Luu D. T., Heizmann P., Dumas C. Pollen-Stigma Adhesion in Kale Is Not Dependent on the Self-(In)Compatibility Genotype. Plant Physiol. 1997 Nov;115(3):1221–1230. doi: 10.1104/pp.115.3.1221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Luu D. T., Marty-Mazars D., Trick M., Dumas C., Heizmann P. Pollen-stigma adhesion in Brassica spp involves SLG and SLR1 glycoproteins. Plant Cell. 1999 Feb;11(2):251–262. doi: 10.1105/tpc.11.2.251. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Mayfield J. A., Fiebig A., Johnstone S. E., Preuss D. Gene families from the Arabidopsis thaliana pollen coat proteome. Science. 2001 Jun 29;292(5526):2482–2485. doi: 10.1126/science.1060972. [DOI] [PubMed] [Google Scholar]
  43. Mayfield J. A., Preuss D. Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat Cell Biol. 2000 Feb;2(2):128–130. doi: 10.1038/35000084. [DOI] [PubMed] [Google Scholar]
  44. Mazina S. E., Matveeva N. P., Ermakov I. P. Determinatsiia polozheniia funktsional'noi pory v pyl'tsevom zerne tabaka. Tsitologiia. 2002;44(1):33–39. [PubMed] [Google Scholar]
  45. Murphy D. J., Ross J. H. Biosynthesis, targeting and processing of oleosin-like proteins, which are major pollen coat components in Brassica napus. Plant J. 1998 Jan;13(1):1–16. [PubMed] [Google Scholar]
  46. Muschietti J., Eyal Y., McCormick S. Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell. 1998 Mar;10(3):319–330. doi: 10.1105/tpc.10.3.319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Nasrallah J. B. Cell-cell signaling in the self-incompatibility response. Curr Opin Plant Biol. 2000 Oct;3(5):368–373. doi: 10.1016/s1369-5266(00)00098-4. [DOI] [PubMed] [Google Scholar]
  48. Nasrallah J. B., Stein J. C., Kandasamy M. K., Nasrallah M. E. Signaling the arrest of pollen tube development in self-incompatible plants. Science. 1994 Dec 2;266(5190):1505–1508. doi: 10.1126/science.266.5190.1505. [DOI] [PubMed] [Google Scholar]
  49. Paxson-Sowders D. M., Dodrill C. H., Owen H. A., Makaroff C. A. DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol. 2001 Dec;127(4):1739–1749. [PMC free article] [PubMed] [Google Scholar]
  50. Preuss D., Lemieux B., Yen G., Davis R. W. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev. 1993 Jun;7(6):974–985. doi: 10.1101/gad.7.6.974. [DOI] [PubMed] [Google Scholar]
  51. Preuss D., Rhee S. Y., Davis R. W. Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science. 1994 Jun 3;264(5164):1458–1460. doi: 10.1126/science.8197459. [DOI] [PubMed] [Google Scholar]
  52. Procissi A., de Laissardière S., Férault M., Vezon D., Pelletier G., Bonhomme S. Five gametophytic mutations affecting pollen development and pollen tube growth in Arabidopsis thaliana. Genetics. 2001 Aug;158(4):1773–1783. doi: 10.1093/genetics/158.4.1773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Pruitt R. E., Vielle-Calzada J. P., Ploense S. E., Grossniklaus U., Lolle S. J. FIDDLEHEAD, a gene required to suppress epidermal cell interactions in Arabidopsis, encodes a putative lipid biosynthetic enzyme. Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1311–1316. doi: 10.1073/pnas.97.3.1311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. ROWLEY J. R., MUEHLETHALER K., FREY-WYSSLING A. A route for the transfer of materials through the pollen grain wall. J Biophys Biochem Cytol. 1959 Dec;6:537–538. doi: 10.1083/jcb.6.3.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Rhee S. Y., Somerville C. R. Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J. 1998 Jul;15(1):79–88. doi: 10.1046/j.1365-313x.1998.00183.x. [DOI] [PubMed] [Google Scholar]
  56. Rhee Seung Y., Osborne Erin, Poindexter Patricia D., Somerville Chris R. Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiol. 2003 Oct 9;133(3):1170–1180. doi: 10.1104/pp.103.028266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Ross J. H., Murphy D. J. Characterization of anther-expressed genes encoding a major class of extracellular oleosin-like proteins in the pollen coat of Brassicaceae. Plant J. 1996 May;9(5):625–637. doi: 10.1046/j.1365-313x.1996.9050625.x. [DOI] [PubMed] [Google Scholar]
  58. Sarker R. H., Elleman C. J., Dickinson H. G. Control of pollen hydration in Brassica requires continued protein synthesis, and glycosylation in necessary for intraspecific incompatibility. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4340–4344. doi: 10.1073/pnas.85.12.4340. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Shayk M., Kolattukudy P. E. Production of a Novel Extracellular Cutinase by the Pollen and the Chemical Composition and Ultrastructure of the Stigma Cuticle of Nasturtium (Tropaeolum majus). Plant Physiol. 1977 Dec;60(6):907–915. doi: 10.1104/pp.60.6.907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Sheldon J. M., Dickinson H. G. Determination of patterning in the pollen wall of Lilium henryi. J Cell Sci. 1983 Sep;63:191–208. doi: 10.1242/jcs.63.1.191. [DOI] [PubMed] [Google Scholar]
  61. Silva N. F., Goring D. R. Mechanisms of self-incompatibility in flowering plants. Cell Mol Life Sci. 2001 Dec;58(14):1988–2007. doi: 10.1007/PL00000832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Spielman M., Preuss D., Li F. L., Browne W. E., Scott R. J., Dickinson H. G. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development. 1997 Jul;124(13):2645–2657. doi: 10.1242/dev.124.13.2645. [DOI] [PubMed] [Google Scholar]
  63. Szibor R., Schubert C., Schöning R., Krause D., Wendt U. Pollen analysis reveals murder season. Nature. 1998 Oct 1;395(6701):449–450. doi: 10.1038/26646. [DOI] [PubMed] [Google Scholar]
  64. Takayama S., Shiba H., Iwano M., Asano K., Hara M., Che F. S., Watanabe M., Hinata K., Isogai A. Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3765–3770. doi: 10.1073/pnas.040580797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Tang Weihua, Ezcurra Inés, Muschietti Jorge, McCormick Sheila. A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell. 2002 Sep;14(9):2277–2287. doi: 10.1105/tpc.003103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Thorsness M. K., Kandasamy M. K., Nasrallah M. E., Nasrallah J. B. Genetic Ablation of Floral Cells in Arabidopsis. Plant Cell. 1993 Mar;5(3):253–261. doi: 10.1105/tpc.5.3.253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Wolters-Arts M., Lush W. M., Mariani C. Lipids are required for directional pollen-tube growth. Nature. 1998 Apr 23;392(6678):818–821. doi: 10.1038/33929. [DOI] [PubMed] [Google Scholar]
  68. Wu G., Gu Y., Li S., Yang Z. A genome-wide analysis of Arabidopsis Rop-interactive CRIB motif-containing proteins that act as Rop GTPase targets. Plant Cell. 2001 Dec;13(12):2841–2856. doi: 10.1105/tpc.010218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  69. Wu Y., Qiu X., Du S., Erickson L. PO149, a new member of pollen pectate lyase-like gene family from alfalfa. Plant Mol Biol. 1996 Dec;32(6):1037–1042. doi: 10.1007/BF00041387. [DOI] [PubMed] [Google Scholar]
  70. Yang C-Y, Spielman M., Coles J. P., Li Y., Ghelani S., Bourdon V., Brown R. C., Lemmon B. E., Scott R. J., Dickinson H. G. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J. 2003 Apr;34(2):229–240. doi: 10.1046/j.1365-313x.2003.01713.x. [DOI] [PubMed] [Google Scholar]
  71. Yang W. C., Sundaresan V. Genetics of gametophyte biogenesis in Arabidopsis. Curr Opin Plant Biol. 2000 Feb;3(1):53–57. doi: 10.1016/s1369-5266(99)00037-0. [DOI] [PubMed] [Google Scholar]
  72. Zinkl G. M., Zwiebel B. I., Grier D. G., Preuss D. Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development. 1999 Dec;126(23):5431–5440. doi: 10.1242/dev.126.23.5431. [DOI] [PubMed] [Google Scholar]

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