Abstract
Lectin receptor-like kinases (Lectin RLKs) are a large family of receptor-like kinases with an extracellular legume lectin-like domain. There are approximately 45 such receptor kinases in Arabidopsis thaliana. Surprisingly, although receptor-like kinases in general are well investigated in Arabidopsis, relatively little is known about the functions of members of the Lectin RLK family. A number of studies implicated members of this family in various functions, such as disease resistance, stress responses, hormone signaling, and legume–rhizobium symbiosis. Our current work demonstrated that mutation in one Lectin RLK gene led to male sterility in Arabidopsis. The sterility was due to defects in pollen development. Pollen development proceeded normally in the mutant until anther stage 8. After that, all pollen grains deformed and collapsed. Mature pollen grains were much smaller than wild-type pollen grains, glued together, and totally collapsed. Therefore, the mutant was named sgc, standing for small, glued-together, and collapsed pollen mutant. The mutant phenotype appeared to be caused by an unidentified sporophytic defect due to the mutation. As revealed by analysis of the promoter-GUS transgenic plants and the gene expression analysis using RT-PCR, the gene showed an interesting temporal and spatial expression pattern: it had no or a low expression in young flowers (roughly before anther stage 6), reached a maximum level around stages 6–7, and then declined gradually to a very low level in young siliques. No expression was detected in microspores or pollen. Together, our data demonstrated that SGC Lectin RLK plays a critical role in pollen development.
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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
Alexander MP (1969) Differential staining of aborted and non-aborted pollen. Stain Technol 44:117–122
Alexander MP (1980) A versatile stain for pollen, fungi, yeast and bacteria. Stain Technol 55:13–18
Barre A, Hervé C, Lescure B, Rougé P (2002) Lectin receptor kinases in plants. Crit Rev Plant Sci 21:379–399
Bergey DR, Orozco-Cardenas M, de Moura DS, Ryan CA (1999) A wound- and systemin-inducible polygalacturonase in tomato leaves. Proc Natl Acad Sci USA 96:1756–1760
Boavida LC, Becker JD, Feijó JA (2005) The making of gametes in higher plants. Int J Dev Biol 49:595–614
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
Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006) A B-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743
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
Consiglio F, Conicella C, Monti L, Carputo D (2003) Highlights of meiotic genes in Arabidopsis thaliana. Afr J Biotechnol 2:516–520
Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137:297–307
Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229
Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rougé P, Pont-Lezica R, Canut H (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140:81–90
He XJ, Zhang ZG, Yan DQ, Zhang JS, Chen SY (2004) A salt-responsive receptor-like kinase gene regulated by the ethylene signaling pathway encodes a plasma membrane serine/threonine kinase. Theor Appl Genet 109:377–383
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
Iwakawa H, Shinmyo A, Sekine M (2006) Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of generative cells in male gametogenesis. Plant J 45:819–831
Jakobsen MK, Poulsen LR, Schulz A, Fleurat-Lessard P, Moller A, Husted S, Schiott M, Amtmann A, Palmgren MG (2005) Pollen development and fertilization in Arabidopsis is dependent on the MALE GAMETOGENESIS IMPAIRED ANTHERS gene encoding a type V P-type ATPase. Genes Dev 19:2757–2769
Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucoronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907
Klimyuk VI, Carroll BJ, Thomas CM, Jones JD (1993) Alkali treatment for rapid preparation of plant material for reliable PCR analysis. Plant J 3:493–494
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434
McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142–S153
Navarro-Gochicoa MT, Camut S, Timmers AC, Niebel A, Herve C, Boutet E, Bono JJ, Imberty A, Cullimore JV (2003) Characterization of four lectin-like receptor kinases expressed in roots of Medicago truncatula. Structure, location, regulation of expression and potential role in the symbiosis with Sinorhizobium meliloti. Plant Physiol 133:1893–1910
Nishiguchi M, Yoshida K, Sumizono T, Tazaki K (2002) A receptor-like protein kinase with a lectin-like domain from lombardy poplar: gene expression in response to wounding and characterization of phosphorylation activity. Mol Genet Genomics 267:506–514
Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799
Peumans WJ, Van Damme EJM (1995) Lectins as plant defense proteins. Plant Physiol 109:347–352
Preuss D, Rhee S, Davis RW (1994) Tetrad analysis possible in Arabidopsis with mutation of the quartet (qrt) genes. Science 264:1458–1460
Rhee SY, Somerville CR (1998) Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. Plant J 15:79–88
Rhee SY, Osborne E, Poindexter PD, Somerville CR (2003) 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 133:v1170–v1180
Riou C, Hervé C, Pacquit V, Dabos P, Lescure B (2002) Expression of an Arabidopsis lectin kinase receptor gene, lecRK-a1, is induced during senescence, wounding and in response to oligogalacturonic acids. Plant Physiol Biochem 40:431–438
Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu Y-C, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16 (Suppl):S46–S60
Shiu S-H, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768
Shiu S-H, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol 132:530–543
Zhao D-Z, Wang G-F, 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
Zuo K, Zhao J, Wang J, Sun X, Tang K (2004) Molecular cloning and characterization of GhlecRK, a novel kinase gene with lectin-like domain from Gossypium hirsutum. DNA Seq 15:58–65
Acknowledgements
We thank the Syngenta Corporation for the T-DNA insertion mutant Garlic_640_F09, and the Salk Institute Genomic Analysis Laboratory and ABRC for the insertion mutants of other Lectin RLK genes. The work was funded by a grant to G. Stacey from the US Department of Energy, Energy Biosciences Program, Office of Basic Energy Sciences (Grant No. DE-FG02-02ER15309).
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Wan, J., Patel, A., Mathieu, M. et al. A lectin receptor-like kinase is required for pollen development in Arabidopsis. Plant Mol Biol 67, 469–482 (2008). https://doi.org/10.1007/s11103-008-9332-6
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DOI: https://doi.org/10.1007/s11103-008-9332-6