Skip to main content
Genetics logoLink to Genetics
. 2004 Aug;167(4):1975–1986. doi: 10.1534/genetics.104.030270

Analysis of transposon insertion mutants highlights the diversity of mechanisms underlying male progamic development in Arabidopsis.

Eric Lalanne 1, Christos Michaelidis 1, James M Moore 1, Wendy Gagliano 1, Andrew Johnson 1, Ramesh Patel 1, Ross Howden 1, Jean-Phillippe Vielle-Calzada 1, Ueli Grossniklaus 1, David Twell 1
PMCID: PMC1471024  PMID: 15342534

Abstract

To identify genes with essential roles in male gametophytic development, including postpollination (progamic) events, we have undertaken a genetic screen based on segregation ratio distortion of a transposon-borne kanamycin-resistance marker. In a population of 3359 Arabidopsis Ds transposon insertion lines, we identified 20 mutants with stably reduced segregation ratios arising from reduced gametophytic transmission. All 20 mutants showed strict cosegregation of Ds and the reduced gametophytic transmission phenotype. Among these, 10 mutants affected both male and female transmission and 10 mutants showed male-specific transmission defects. Four male and female (ungud) mutants and 1 male-specific mutant showed cellular defects in microspores and/or in developing pollen. The 6 remaining ungud mutants and 9 male-specific (seth) mutants affected pollen functions during progamic development. In vitro and in vivo analyses are reported for 5 seth mutants. seth6 completely blocked pollen germination, while seth7 strongly reduced pollen germination efficiency and tube growth. In contrast, seth8, seth9, or seth10 pollen showed reduced competitive ability that was linked to slower rates of pollen tube growth. Gene sequences disrupted in seth insertions suggest essential functions for putative SETH proteins in diverse processes including protein anchoring, cell wall biosynthesis, signaling, and metabolism.

Full Text

The Full Text of this article is available as a PDF (330.9 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alexander M. P. Differential staining of aborted and nonaborted pollen. Stain Technol. 1969 May;44(3):117–122. doi: 10.3109/10520296909063335. [DOI] [PubMed] [Google Scholar]
  2. Bonhomme S., Horlow C., Vezon D., de Laissardière S., Guyon A., Férault M., Marchand M., Bechtold N., Pelletier G. T-DNA mediated disruption of essential gametophytic genes in Arabidopsis is unexpectedly rare and cannot be inferred from segregation distortion alone. Mol Gen Genet. 1998 Dec;260(5):444–452. doi: 10.1007/s004380050915. [DOI] [PubMed] [Google Scholar]
  3. Chen Y. C., McCormick S. sidecar pollen, an Arabidopsis thaliana male gametophytic mutant with aberrant cell divisions during pollen development. Development. 1996 Oct;122(10):3243–3253. doi: 10.1242/dev.122.10.3243. [DOI] [PubMed] [Google Scholar]
  4. Christensen C. A., Subramanian S., Drews G. N. Identification of gametophytic mutations affecting female gametophyte development in Arabidopsis. Dev Biol. 1998 Oct 1;202(1):136–151. doi: 10.1006/dbio.1998.8980. [DOI] [PubMed] [Google Scholar]
  5. Dolferus R., Van den Bossche D., Jacobs M. Sequence analysis of two null-mutant alleles of the single Arabidopsis Adh locus. Mol Gen Genet. 1990 Nov;224(2):297–302. doi: 10.1007/BF00271565. [DOI] [PubMed] [Google Scholar]
  6. Estruch J. J., Kadwell S., Merlin E., Crossland L. Cloning and characterization of a maize pollen-specific calcium-dependent calmodulin-independent protein kinase. Proc Natl Acad Sci U S A. 1994 Sep 13;91(19):8837–8841. doi: 10.1073/pnas.91.19.8837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Goff Stephen A., Ricke Darrell, Lan Tien-Hung, Presting Gernot, Wang Ronglin, Dunn Molly, Glazebrook Jane, Sessions Allen, Oeller Paul, Varma Hemant. A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science. 2002 Apr 5;296(5565):92–100. doi: 10.1126/science.1068275. [DOI] [PubMed] [Google Scholar]
  8. Golovkin Maxim, Reddy Anireddy S. N. A calmodulin-binding protein from Arabidopsis has an essential role in pollen germination. Proc Natl Acad Sci U S A. 2003 Aug 19;100(18):10558–10563. doi: 10.1073/pnas.1734110100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Goubet Florence, Misrahi Audrey, Park Soon Ki, Zhang Zhinong, Twell David, Dupree Paul. AtCSLA7, a cellulose synthase-like putative glycosyltransferase, is important for pollen tube growth and embryogenesis in Arabidopsis. Plant Physiol. 2003 Feb;131(2):547–557. doi: 10.1104/pp.014555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Grossniklaus U., Vielle-Calzada J. P., Hoeppner M. A., Gagliano W. B. Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science. 1998 Apr 17;280(5362):446–450. doi: 10.1126/science.280.5362.446. [DOI] [PubMed] [Google Scholar]
  12. Gupta Rajeev, Ting Julie T. L., Sokolov Lubomir N., Johnson Sheila A., Luan Sheng. A tumor suppressor homolog, AtPTEN1, is essential for pollen development in Arabidopsis. Plant Cell. 2002 Oct;14(10):2495–2507. doi: 10.1105/tpc.005702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hepler P. K., Vidali L., Cheung A. Y. Polarized cell growth in higher plants. Annu Rev Cell Dev Biol. 2001;17:159–187. doi: 10.1146/annurev.cellbio.17.1.159. [DOI] [PubMed] [Google Scholar]
  14. Honys David, Twell David. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol. 2003 Jun;132(2):640–652. doi: 10.1104/pp.103.020925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Howden R., Park S. K., Moore J. M., Orme J., Grossniklaus U., Twell D. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics. 1998 Jun;149(2):621–631. doi: 10.1093/genetics/149.2.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Huck Norbert, Moore James M., Federer Michael, Grossniklaus Ueli. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development. 2003 May;130(10):2149–2159. doi: 10.1242/dev.00458. [DOI] [PubMed] [Google Scholar]
  17. Ingersoll J. C., Rothenberg M., Liedl B. E., Folkerts K., Garvin D., Hanson M. R., Doyle J. J., Mutschler M. A. A novel anther-expressed adh-homologous gene in Lycopersicon esculentum. Plant Mol Biol. 1994 Dec;26(6):1875–1891. doi: 10.1007/BF00019500. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. Kang Byung-Ho, Rancour David M., Bednarek Sebastian Y. The dynamin-like protein ADL1C is essential for plasma membrane maintenance during pollen maturation. Plant J. 2003 Jul;35(1):1–15. doi: 10.1046/j.1365-313x.2003.01775.x. [DOI] [PubMed] [Google Scholar]
  21. Karni Leah, Aloni Beny. Fructokinase and hexokinase from pollen grains of bell pepper (Capsicum annuum L.): possible role in pollen germination under conditions of high temperature and CO2 enrichment. Ann Bot. 2002 Nov;90(5):607–612. doi: 10.1093/aob/mcf234. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Lalanne Eric, Honys David, Johnson Andrew, Borner Georg H. H., Lilley Kathryn S., Dupree Paul, Grossniklaus Ueli, Twell David. SETH1 and SETH2, two components of the glycosylphosphatidylinositol anchor biosynthetic pathway, are required for pollen germination and tube growth in Arabidopsis. Plant Cell. 2003 Dec 11;16(1):229–240. doi: 10.1105/tpc.014407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Liu Y. G., Mitsukawa N., Oosumi T., Whittier R. F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 1995 Sep;8(3):457–463. doi: 10.1046/j.1365-313x.1995.08030457.x. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Mellema Stefan, Eichenberger Waldemar, Rawyler André, Suter Marianne, Tadege Million, Kuhlemeier Cris. The ethanolic fermentation pathway supports respiration and lipid biosynthesis in tobacco pollen. Plant J. 2002 May;30(3):329–336. doi: 10.1046/j.1365-313x.2002.01293.x. [DOI] [PubMed] [Google Scholar]
  28. Moore J. M., Calzada J. P., Gagliano W., Grossniklaus U. Genetic characterization of hadad, a mutant disrupting female gametogenesis in Arabidopsis thaliana. Cold Spring Harb Symp Quant Biol. 1997;62:35–47. [PubMed] [Google Scholar]
  29. Motchoulski A., Liscum E. Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. Science. 1999 Oct 29;286(5441):961–964. doi: 10.1126/science.286.5441.961. [DOI] [PubMed] [Google Scholar]
  30. Mouline Karine, Véry Anne-Aliénor, Gaymard Frédéric, Boucherez Jossia, Pilot Guillaume, Devic Martine, Bouchez David, Thibaud Jean-Baptiste, Sentenac Hervé. Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. Genes Dev. 2002 Feb 1;16(3):339–350. doi: 10.1101/gad.213902. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Muschietti J., Dircks L., Vancanneyt G., McCormick S. LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J. 1994 Sep;6(3):321–338. doi: 10.1046/j.1365-313x.1994.06030321.x. [DOI] [PubMed] [Google Scholar]
  32. Neuteboom L. W., Ng J. M., Kuyper M., Clijdesdale O. R., Hooykaas P. J., van der Zaal B. J. Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol. 1999 Jan;39(2):273–287. doi: 10.1023/a:1006104205959. [DOI] [PubMed] [Google Scholar]
  33. Page Damian R., Grossniklaus Ueli. The art and design of genetic screens: Arabidopsis thaliana. Nat Rev Genet. 2002 Feb;3(2):124–136. doi: 10.1038/nrg730. [DOI] [PubMed] [Google Scholar]
  34. Palanivelu Ravishankar, Brass Laura, Edlund Anna F., Preuss Daphne. Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell. 2003 Jul 11;114(1):47–59. doi: 10.1016/s0092-8674(03)00479-3. [DOI] [PubMed] [Google Scholar]
  35. Park S. K., Howden R., Twell D. The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development. 1998 Oct;125(19):3789–3799. doi: 10.1242/dev.125.19.3789. [DOI] [PubMed] [Google Scholar]
  36. Park S. K., Twell D. Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen1 mutant. Plant Physiol. 2001 Jun;126(2):899–909. doi: 10.1104/pp.126.2.899. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Pego J. V., Smeekens S. C. Plant fructokinases: a sweet family get-together. Trends Plant Sci. 2000 Dec;5(12):531–536. doi: 10.1016/s1360-1385(00)01783-0. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Rotman Nicolas, Rozier Frédérique, Boavida Leonor, Dumas Christian, Berger Frédéric, Faure Jean-Emmanuel. Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol. 2003 Mar 4;13(5):432–436. doi: 10.1016/s0960-9822(03)00093-9. [DOI] [PubMed] [Google Scholar]
  41. Sakai T., Wada T., Ishiguro S., Okada K. RPT2. A signal transducer of the phototropic response in Arabidopsis. Plant Cell. 2000 Feb;12(2):225–236. doi: 10.1105/tpc.12.2.225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Sanderfoot A. A., Pilgrim M., Adam L., Raikhel N. V. Disruption of individual members of Arabidopsis syntaxin gene families indicates each has essential functions. Plant Cell. 2001 Mar;13(3):659–666. doi: 10.1105/tpc.13.3.659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Schomburg Fritz M., Bizzell Colleen M., Lee Dong Ju, Zeevaart Jan A. D., Amasino Richard M. Overexpression of a novel class of gibberellin 2-oxidases decreases gibberellin levels and creates dwarf plants. Plant Cell. 2003 Jan;15(1):151–163. doi: 10.1105/tpc.005975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Sessions Allen, Burke Ellen, Presting Gernot, Aux George, McElver John, Patton David, Dietrich Bob, Ho Patrick, Bacwaden Johana, Ko Cynthia. A high-throughput Arabidopsis reverse genetics system. Plant Cell. 2002 Dec;14(12):2985–2994. doi: 10.1105/tpc.004630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Singh Davinder P., Jermakow Angelica M., Swain Stephen M. Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell. 2002 Dec;14(12):3133–3147. doi: 10.1105/tpc.003046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Steinebrunner Iris, Wu Jian, Sun Yu, Corbett Ashley, Roux Stanley J. Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol. 2003 Apr;131(4):1638–1647. doi: 10.1104/pp.102.014308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Sundaresan V., Springer P., Volpe T., Haward S., Jones J. D., Dean C., Ma H., Martienssen R. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev. 1995 Jul 15;9(14):1797–1810. doi: 10.1101/gad.9.14.1797. [DOI] [PubMed] [Google Scholar]
  48. 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]
  49. Twell David, Park Soon Ki, Hawkins Timothy J., Schubert Daniel, Schmidt Renate, Smertenko Andrei, Hussey Patrick J. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nat Cell Biol. 2002 Sep;4(9):711–714. doi: 10.1038/ncb844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Tzeng Yih-Ling, Datta Anup, Strole Christy, Kolli V. S. Kumar, Birck Matthew R., Taylor William P., Carlson Russell W., Woodard Ronald W., Stephens David S. KpsF is the arabinose-5-phosphate isomerase required for 3-deoxy-D-manno-octulosonic acid biosynthesis and for both lipooligosaccharide assembly and capsular polysaccharide expression in Neisseria meningitidis. J Biol Chem. 2002 Apr 15;277(27):24103–24113. doi: 10.1074/jbc.M200931200. [DOI] [PubMed] [Google Scholar]
  51. Wilhelmi L. K., Preuss D. Self-sterility in Arabidopsis due to defective pollen tube guidance. Science. 1996 Nov 29;274(5292):1535–1537. doi: 10.1126/science.274.5292.1535. [DOI] [PubMed] [Google Scholar]
  52. da Costa-Nunes José António, Grossniklaus Ueli. Unveiling the gene-expression profile of pollen. Genome Biol. 2003 Dec 24;5(1):205–205. doi: 10.1186/gb-2003-5-1-205. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES