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About 10% of the genes in plants are specifically or selectively expressed in pollen, but the functions of most are not understood. We used Arabidopsis to identify mutants that are defective at a particular stage of pollen development, or during pollen hydration, pollen tube growth, pollen tube guidance, or fertilization. Usually such mutants have altered transmission through the male parent, but do not affect female transmission, so can be studied in heterozygotes.

 

 

We were interested in double fertilization, specifically in how the two sperm and their fusion partners, the egg and the central cell, recognize and fuse with each other. To develop tools for this objective, we generated cDNA libraries from maize sperm, eggs, and embryo sacs, sequenced ~20,000 ESTs, then used these datasets as starting points to identify gamete-specific genes. We identified promoter elements that will drive gamete-specific gene expression. We then used Arabidopsis to identify T-DNA insertions in gamete-expressed genes, and tested whether there was a phenotype. We found that fertilization fails when some of these genes were disrupted.

 

 

 

 

 

 

 

 

 

 

 

 

 

Jiang H, Yi J, Boavida LC, Chen Y, Becker JD, Köhler C, McCormick S. 2015. Intercellular communication in pollen discovered via AHG3 transcript movement from the vegetative cell to sperm. Proc Natl Acad Sci USA 112:13378-83. https://doi.org/10.1073/pnas.1510854112

Gui, C., Dong, X., Liu, H., Huang, W., Zhang, D., Wang, S., Barberini, M.L., Gao, X., Muschietti, J., McCormick, S. and Tang, W. 2014. Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbing mode. Plant Cell 26: 3538-3555. https://doi.org/10.1105/tpc.114.127381

Huang, W., Liu, H., McCormick, S., and Tang, W. 2014. Tomato pistil factor LeSTIG1 promotes in vivo pollen tube growth by binding to phosphatidylinositol 3-phosphate and the extracellular domain of LePRK2. Plant Cell 26: 2505-2523. https://doi.org/10.1105/tpc.114.123281

Zheng, B., He, H., Zheng, Y., Wu, W. and McCormick, S. 2014. An ARID domain-containing protein within nuclear bodies is required for sperm cell formation in Arabidopsis thaliana. PLoS Genetics https://doi.org/10.1371/journal.pgen.1004421

McCormick, S. 2013. Pollen. Current Biology 23: R988-R990; doi: 10.1016/j.cub.2013.08.016 

Zhao, X-Y., Wang, Q., Li., S., Ge., F-R., Zhou, L-Z.,  McCormick, S. and Zhang, Y. 2013. The juxtamembrane and carboxy-terminal domains of Arabidopsis PRK2 are critical for ROP-induced growth in pollen tubes. J. Experimental Botany 64: 5599-5610. https://doi.org/10.1093/jxb/ert323

Boavida, L.C., Qin, P., Broz, M., Becker, J.D. and McCormick, S. 2013. Arabidopsis tetraspanins are confined to discrete expression domains and cell types in reproductive tissues and form homo- and hetero-dimers when expressed in yeast. Plant Physiology 163: 696-712. https://doi.org/10.1104/pp.113.216598

Li, S., Zhou, L-Z., Feng, Q-N., McCormick, S. and Zhang, Y. 2013. The C-terminal hypervariable domain targets Arabidopsis ROP9 to the invaginated pollen tube plasma membrane. Molecular Plant  6:1362-1364. https://doi.org/10.1093/mp/sst098 

Scarpin, R., Sigaut, L., Pietrasanta, L., McCormick, S., Zheng, B. and Muschietti, J. 2013. Cajal bodies are developmentally regulated during pollen development and pollen tube growth in Arabidopsis thaliana. Molecular Plant 6:1355-1357. https://doi.org/10.1093/mp/sst077 

 

Loraine, A.E., McCormick, S., Estrada, A., Patel, K. and Qin, P. 2013.  RNA-Seq of Arabidopsis thaliana pollen uncovers novel transcription and alternative splicing. Plant Physiology 162:1092-1109. https://doi.org/10.1104/pp.112.211441 

 

Li, S., Ge, F-R., Xu, M., Zhao, X-Y., Huang, G-Q., Zhou, L-Zi., Wang, J-G., Kombrink, A., McCormick, S., Zhang, X.S. and Zhang, Y. 2013. Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. Plant Journal 74: 486–497. https://doi.org/10.1111/tpj.12139 

 

Qin, P., Ting, D., Shieh, A. and McCormick, S. 2012. Callose plug deposition patterns vary in pollen tubes of Arabidopsis thaliana ecotypes and in tomato species. BMC Plant Biology 12: 178. https://doi.org/10.1186/1471-2229-12-178 

 

Zhang, Y., Li, S., Zhou, L-Z., Fox, E., Pao, J., Sun, W, Zhou, C. and McCormick, S. 2011. Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics. Plant Journal 68:1081-1092.  https://doi.org/10.1111/j.1365-313X.2011.04761.x

 

Alandete-Saez, M., Ron, M., Leiboff, S. and McCormick, S. 2011. GEX1 has dual functions in gametophyte development and early embryogenesis. Plant Journal 68: 620-632. https://doi.org/10.1111/j.1365-313X.2011.04713.x

 

Zheng, B., Chen, X. and McCormick, S. 2011. The anaphase-promoting complex/cyclosome is a dual integrator that regulates both miRNA-mediated transcriptional regulation of Cyclin B1 and degradation of Cyclin B1 during Arabidopsis male gametophyte development. Plant Cell 23: 1033-1046. https://doi.org/10.1105/tpc.111.083980

Ron, M., Alandete-Saez, M., Williams, L., Fletcher, J. and McCormick, S. 2010. Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes & Development 24:1010-1021. http://www.genesdev.org/cgi/doi/10.1101/gad.1882810

Muschietti, J. and McCormick, S. 2010. Abscisic acid (ABA) receptors: light at the end of the tunnel. F1000 Biology Reports 2:15 http://f1000biology.com/reports/10.3410/B2-15/

Zhang, Y.*, He, J.*, Lee, D. and McCormick, S. 2010. Interdependence of endomembrane trafficking and actin dynamics during polarized growth of Arabidopsis pollen tubes. Plant Physiology 152:2200-2210.  * co-first authors. https://doi.org/10.1104/pp.109.142349

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 Biology 10:33 (http://www.biomedcentral.com/1471-2229/10/33)

Zhang, Y. and McCormick, S. 2009. The regulation of vesicle trafficking by small GTPases and phospholipids during pollen tube growth. Sexual Plant Reproduction 23:87-93. https://doi:10.1007/s00497-009-0118-z.

Zhang, Y. and McCormick, S. 2009. AGC VIII kinases: at the crossroads of cellular signaling. Trends in Plant Science 14: 689-695.

Boavida, L.C., Shuai, B., Yu, H-J., Pagnussat, G. C., Sundaresan, V. and McCormick, S. 2009. A collection of Ds insertions associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 181: 1369-1385. https://doi.org/10.1534/genetics.108.090852

Zhang, Y., He, J. and McCormick,S. 2009. Two Arabidopsis AGC kinases are critical for the polarized growth of pollen tubes. Plant Journal 58: 474-484. https://doi.org/10.1111/j.1365-313X.2009.03792.x 

 

Wang, H., Boavida, L.C., Ron, M. and McCormick, S. 2008. Truncation of a protein disulfide isomerase, PDIL2-1, delays embryo sac maturation and disrupts pollen tube guidance in Arabidopsis thaliana. Plant Cell 20: 3300-3311. https://doi.org/10.1105/tpc.108.062919

Zhang, D., Wengier, D., Shuai, B., Gui, C.P., Muschietti, J., McCormick, S. and Tang,W.H. 2008. The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth. Plant Physiology 148: 1368-1379. https://doi.org/10.1104/pp.108.124420

Blanvillain, R., Boavida, L.C., McCormick, S. and Ow, D.W. 2008. Exportin1 genes are essential for development and function of the gametophytes in Arabidopsis thaliana. Genetics 180: 1493-1500; 10.1534/genetics.108.094896.

Borges, F., Gomes, G., Gardner,R., Moreno, N., McCormick, S., Feijo, J.A. and Becker, J.D. 2008. Comparative transcriptomics of Arabidopsis thaliana sperm cells. Plant Physiology 148: 1168-1181; 10.1104/pp.108.125229.

Alandete-Saez, M., Ron, M. and McCormick, S. 2008. GEX3, expressed in the male gametophyte and in the egg cell of Arabidopsis thaliana, is essential for micropylar pollen tube guidance and plays a role during early embryogenesis. Molecular Plant 1: 586-598.

Zhang, Y and McCormick, S. 2007. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 18830-18835.

Boavida, L.C. and McCormick, S. 2007. Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant Journal 52: 570-582. https://doi.org/10.1111/j.1365-313X.2007.03248.x

McCormick, S. 2007. Reproductive dialog. Science 317: 606-607.

Yang, H., Kaur, N., Kiriakopolos, S. and McCormick, S. 2006. EST generation and analyses towards identifying female gametophyte-specific genes in Zea mays L. Planta 224: 1004-1014.

Holmes-Davis, R., Tanaka, C.K., Vensel, W., Hurkman, W. and McCormick, S. 2005. Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5: 4864-4884.

Engel, M.L., Holmes-Davis, R. and McCormick, S. 2005. Green sperm. Identification of male gamete promoters in Arabidopsis thaliana. Plant Physiology 138: 2124-2133.

McCormick, S. and Yang, H. 2005. Is there more than one way to attract a pollen tube? Trends Plant Sciences 10: 260-263.

Kaothien, P., Ok, S.H., Shuai, B., Wengier, D., Cotter, R., Kelley, D., Kiriakopolos, S., Muschietti, J. and McCormick, S. 2005. Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth. Plant Journal 42: 492-503.

Wang, Y., Magnard, J-L., McCormick, S. and Yang, M. 2004. Progression through meiosis I and meiosis II in Arabidopsis thaliana anthers is regulated by an A-type cyclin predominately expressed in prophase I. Plant Physiology 136: 4127-4135.

Johnson-Brousseau, S.A. and McCormick, S. 2004. A compendium of methods useful for characterizing Arabidopsis pollen mutants and gametophytically-expressed genes. Plant Journal 39: 761-775. https://doi.org/10.1111/j.1365-313X.2004.02147.x

Guyon, V., Tang, W., Monti., M., Raiola, A., DeLorenzo, G., McCormick, S. and Taylor, L. 2004. Antisense phenotypes reveal a role for SHY, a pollen-specific leucine-rich repeat protein, in pollen tube growth. Plant Journal 39: 643-654.

Tang, W., Kelley, D., Ezcurra, I., Cotter, R. and McCormick, S. 2004. LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant Journal 39: 343-353.

McCormick, S. 2004. Control of male gametophyte development. Plant Cell 16: S142-153.

Wengier, D., Valsecchi, I., Cabanas, M.L., Tang, W., McCormick, S. and Muschietti, J. 2003. The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc. Natl. Acad. Sci. USA 100:6860-6865. https://doi.org/10.1073/pnas.0631728100

Engel, M.L., Chaboud, A., Dumas, C. and McCormick, S. 2003. Sperm cells of Zea mays have a complex complement of mRNAs. Plant Journal 34:697-707. https://doi.org/10.1046/j.1365-313X.2003.01761.x

Tang, W., Ezcurra, I., Muschietti, J. and McCormick, S. 2002. A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 14: 2277-2287. https://doi.org/10.1105/tpc.003103

Yang, M. and McCormick, S. 2002. The Arabidopsis thaliana MEI1 gene likely encodes a protein with BRCT domains. Sexual Plant Reproduction 14:355-357. https://doi.org/10.1007/s00497-002-0129-5

Kim, H-Y., Cotter, R., Johnson, S., Senda, M., Dodds, P., Kulikauskas, R., Tang, W., Ezcurra, I., Herzmark, P. and McCormick, S. 2002. New pollen-specific receptor kinases identified in tomato, maize and Arabidopsis: the tomato kinases show overlapping but distinct localization patterns on pollen tubes. Plant Molecular Biology 50:1-16. https://doi.org/10.1023/A:1016077014583

Cock, J.M. and McCormick, S. 2001. A large family of genes that share homology with CLAVATA3. Plant Physiology 126: 939-943. https://doi.org/10.1104/pp.126.3.939

Magnard, J-L., Yang, M., Chen, Y-C. S., Leary, M. and McCormick, S. 2001 The Arabidopsis thaliana gene Tardy Asynchronous Meiosis (TAM) is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiology 127:1157-1166. https://doi.org/10.1104/pp.010473

Johnson, S. and McCormick, S. 2001. Pollen germinates precociously in the anthers of raring-to-go, an Arabidopsis thaliana gametophytic mutant. Plant Physiology 126: 685-695. https://doi.org/10.1104/pp.126.2.685