Abstract
We have previously described the FERTILIZATION-RELATED KINASE 2 (ScFRK2), a MAP kinase kinase kinase from Solanum chacoense that is predominantly expressed in reproductive tissues. Overexpression of the ScFRK2 gene modifies the cell fate of ovule initials and induces homeotic transformation of ovules into carpelloid structures. Since the ScFRK2 gene is normally expressed also in anthers, we now further our observations on the effect of ScFRK2 overexpression in male reproductive structures. Although ScFRK2 mRNA levels detected by RNA blot were relatively constant during early anther development, there was a dramatic change in tissue distribution of ScFRK2 mRNA when detected by in situ RNA hybridization. In the young anther, ScFRK2 mRNA accumulated mainly in microsporocytes and tapetum. By the time of anthesis, ScFRK2 mRNA was no longer found in degenerating tapetum or pollen grains but instead found abundantly on the anther wall, including epidermis and endothecium. Overexpression of ScFRK2 transcripts strongly disturbed pollen development. At maturity, almost two-thirds of pollen grains were severely affected and non-viable, while the remaining pollen grains were significantly smaller than wild type pollen. Cross with pollen from a ScFRK2 overexpression line into a wild type female plant produced an F1 population with 44% of the progeny having the transgene, suggesting that the pollen defect is caused by a sporophytic dysfunction, leading to major structural defects and incomplete pollen development.
Similar content being viewed by others
Abbreviations
- DPA:
-
Days post anthesis
- FRK:
-
Fertilization-related kinase
- LRR:
-
Leucine-rich repeat
- MAPKKK:
-
Mitogen-activated protein kinase kinase kinase
- SEM:
-
Scanning electron microscopy
- TEM:
-
Transmission electron microscopy
References
Albrecht C, Russinova E, Hecht V, Baaijens E, de Vries S (2005) The Arabidopsis thaliana SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASES1 and 2 control male sporogenesis. Plant Cell 17:3337–3349
Boavida LC, Becker JD, Feijo JA (2005) The making of gametes in higher plants. Int J Dev Biol 49:595–614
Bowman J (1994) Arabidopsis: an atlas of morphology and development. Springer, Berlin Heidelberg New York
Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727
Colcombet J, Boisson-Dernier A, Ros-Palau R, Vera CE, Schroeder JI (2005) Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASES1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17:3350–3361
Esau K (1977) Anatomy of seed plants. Wiley, New York
Germain H, Rudd S, Zotti C, Caron S, O’Brien M, Chantha SC, Lagace M, Major F, Matton DP (2005) A 6374 unigene set corresponding to low abundance transcripts expressed following fertilization in solanum chacoense bitt, and characterization of 30 receptor-like kinases. Plant Mol Biol 59:515–532
Gray-Mitsumune M, O’Brien M, Bertrand C, Tebbji F, Nantel A, Matton DP (2006) Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense. J Exp Bot (In press). DOI 10.1093/jxb/erl194
Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant Physiol 127:803–816
Hord CL, Chen C, Deyoung BJ, Clark SE, Ma H (2006) The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18:1667–1680
Johnson MA, Preuss D (2003) On your mark, get set, GROW! LePRK2-LAT52 interactions regulate pollen tube growth. Trends Plant Sci 8:97–99
Jones JDG, Dunsmuir P, Bedbrook J (1985) High level expression of introduced chimeric genes in regenerated transformed plants. EMBO J 4:2411–2418
Jung KH, Han MJ, Lee YS, Kim YW, Hwang I, Kim MJ, Kim YK, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722
Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different Temporal and Spatial Gene Expression Patterns Occur during Anther Development. Plant Cell 2:1201–1224
Lantin S, O’Brien M, Matton DP (1999) Pollination, wounding and jasmonate treatments induce the expression of a developmentally regulated pistil dioxygenase at a distance, in the ovary, in the wild potato Solanum chacoense Bitt. Plant Mol Biol 41:371–386
Lee HS, Karunanandaa B, McCubbin A, Gilroy S, Kao Th (1996) PRK1, a receptor-like kinase of Petunia inflata, is essential for postmeiotic development of pollen. Plant J 9:613–624
Lee HS, Chung YY, Das C, Karunanandaa B, van Went JL, Mariani C, Kao TH (1997) Embryo sac development is affected in Petunia inflata plants transformed with an antisense gene encoding the extracellular domain of receptor kinase PRK1. Sex Plant Reprod 10:341–350
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434
Muschietti J, Dircks L, Vancanneyt G, McCormick S (1994) LAT52 protein is essential for tomato pollen development: pollen expressing antisense LAT52 RNA hydrates and germinates abnormally and cannot achieve fertilization. Plant J 6:321–338
Nonomura K, Miyoshi K, Eiguchi M, Suzuki T, Miyao A, Hirochika H, Kurata N (2003) The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15:1728–1739
Preston J, Wheeler J, Heazlewood J, Li SF, Parish RW (2004) AtMYB32 is required for normal pollen development in Arabidopsis thaliana. Plant J 40:979–995
Schmidt ED, Guzzo F, Toonen MA, de Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell Suppl(16):S46–S60
Sheridan WF, Golubeva EA, Abrhamova LI, Golubovskaya IN (1999) The mac1 mutation alters the developmental fate of the hypodermal cells and their cellular progeny in the maize anther. Genetics 153:933–941
Sorensen A, Guerineau F, Canales-Holzeis C, Dickinson HG, Scott RJ (2002) A novel extinction screen in Arabidopsis thaliana identifies mutant plants defective in early microsporangial development. Plant J 29:581–594
Sorensen AM, Krober S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423
Tang W, Ezcurra I, Muschietti J, 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
Wilson ZA, Yang C (2004) Plant gametogenesis: conservation and contrasts in development. Reproduction 128:483–492
Wilson ZA, Morroll SM, Dawson J, Swarup R, Tighe PJ (2001) The arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant J 28:27–39
Yang SL, Xie LF, Mao HZ, Puah CS, Yang WC, Jiang L, Sundaresan V, Ye D (2003) Tapetum determinant 1 is required for cell specialization in the arabidopsis anther. Plant Cell 15:2792–2804
Zhang Y, Shewry PR, Jones H, Barcelo P, Lazzeri PA, Halford NG (2001) Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley. Plant J 28:431–441
Zhang W, Sun Y, Timofejeva L, Chen C, Grossniklaus U, Ma H (2006) Regulation of arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133:3085–3095
Zhao DZ, Wang GF, Speal B, Ma H (2002) The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the arabidopsis anther. Genes Dev 16:2021–2031
Acknowledgments
We thank Gabriel Téodorescu for plant care and maintenance. M. O’Brien is the recipient of Ph. D. fellowships from the Natural Sciences and Engineering Research Council of Canada (NSERC) and from Le Fonds Québécois de la Recherche sur la Nature et les Technologies (FQRNT, Québec), and C. Kapfer is the recipient of a M. Sc. fellowship from NSERC. D.P. Matton holds a Canada Research Chair in Functional Genomics and Plant Signal Transduction.
Author information
Authors and Affiliations
Corresponding author
Additional information
Martin O’Brien and Madoka Gray-Mitsumune contributed equally to this work.
Rights and permissions
About this article
Cite this article
O’Brien, M., Gray-Mitsumune, M., Kapfer, C. et al. The ScFRK2 MAP kinase kinase kinase from Solanum chacoense affects pollen development and viability . Planta 225, 1221–1231 (2007). https://doi.org/10.1007/s00425-006-0432-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-006-0432-8