Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Successful fertilization depends on active molecular dialogues that the male gametophyte can establish with the pistil and the female gametophyte. Pollen grains and stigmas must recognize each other; pollen tubes need to identify the pistil tissues they will penetrate, follow positional cues to exit the transmitting tract and finally, locate the ovules. These molecular dialogues directly affect pollen tube growth rate and orientation. Receptor-like kinases (RLKs) are natural candidates for the perception and decoding of extracellular signals and their transduction to downstream cytoplasmic interactors. Here, we update knowledge regarding how RLKs are involved in pollen tube growth, cell wall integrity and guidance. In addition, we use public data to build a pollen tube RLK interactome that might help direct experiments to elucidate the function of pollen RLKs and their associated proteins. © 2017 Elsevier Ltd

Registro:

Documento: Artículo
Título:How many receptor-like kinases are required to operate a pollen tube
Autor:Muschietti, J.P.; Wengier, D.L.
Filiación:Instituto de Investigaciones en Ingeniería Genética y Biología Molecular, Dr. Héctor Torres (INGEBI-CONICET), Vuelta de Obligado 2490, Buenos Aires, C1428ADN, Argentina
Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Int. Güiraldes 2160, Ciudad Universitaria, Pabellón II, Buenos Aires, C1428EGA, Argentina
Palabras clave:Arabidopsis protein; cell surface receptor; protein serine threonine kinase; Arabidopsis; enzymology; flower; genetics; growth, development and aging; metabolism; ovule; pollen; pollen tube; pollination; Arabidopsis; Arabidopsis Proteins; Flowers; Ovule; Pollen; Pollen Tube; Pollination; Protein-Serine-Threonine Kinases; Receptors, Cell Surface
Año:2018
Volumen:41
Página de inicio:73
Página de fin:82
DOI: http://dx.doi.org/10.1016/j.pbi.2017.09.008
Título revista:Current Opinion in Plant Biology
Título revista abreviado:Curr. Opin. Plant Biol.
ISSN:13695266
CODEN:COPBF
CAS:protein serine threonine kinase; Arabidopsis Proteins; Protein-Serine-Threonine Kinases; Receptors, Cell Surface
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_13695266_v41_n_p73_Muschietti

Referencias:

  • Cheung, A.Y., Wu, H.M., Structural and signaling networks for the polar cell growth machinery in pollen tubes (2008) Annu Rev Plant Biol, 59, pp. 547-572
  • Shiu, S.H., Bleecker, A.B., Plant receptor-like kinase gene family: diversity, function, and signaling (2001) Sci STKE, 2001, p. re22
  • Boisson-Dernier, A., Roy, S., Kritsas, K., Grobei, M.A., Jaciubek, M., Schroeder, J.I., Grossniklaus, U., Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge (2009) Development, 136, pp. 3279-3288
  • Miyazaki, S., Murata, T., Sakurai-Ozato, N., Kubo, M., Demura, T., Fukuda, H., Hasebe, M., ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization (2009) Curr Biol, 19, pp. 1327-1331
  • Takeuchi, H., Higashiyama, T., Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis (2016) Nature, 531, pp. 245-248. , This study together with [6] demonstrates that the LURE1 peptide binds to redundant pollen tube RLKs involved in ovule targeting
  • Wang, T., Liang, L., Xue, Y., Jia, P.-F., Chen, W., Zhang, M.-X., Wang, Y.-C., Yang, W.-C., A receptor heteromer mediates the male perception of female attractants in plants (2016) Nature, 531, pp. 241-244. , See annotation to Ref. [5]
  • Borassi, C., Sede, A.R., Mecchia, M.A., Salgado Salter, J.D., Marzol, E., Muschietti, J.P., Estevez, J.M., An update on cell surface proteins containing extensin-motifs (2016) J Exp Bot, 67, pp. 477-487
  • Huang, J., Zhang, T., Linstroth, L., Tillman, Z., Otegui, M.S., Owen, H.A., Zhao, D., Control of anther cell differentiation by the small protein ligand TPD1 and its receptor EMS1 in Arabidopsis (2016) PLoS Genet, 12, p. e1006147. , This study shows that the small secreted cysteine-rich protein ligand (TPD1) and the RLK (EMS1) pair, control tapetal cell differentiation
  • Van der Does, D., Boutrot, F., Engelsdorf, T., Rhodes, J., McKenna, J.F., Vernhettes, S., Koevoets, I., Miedes, E., The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses (2017) PLoS Genet, 13, p. e1006832. , In this report, the receptor-like kinase MIK2 senses cell wall integrity regulating plant growth and adaptation to abiotic and biotic stresses
  • Julkowska, M.M., Klei, K., Fokkens, L., Haring, M.A., Schranz, M.E., Testerink, C., Natural variation in rosette size under salt stress conditions corresponds to developmental differences between Arabidopsis accessions and allelic variation in the LRR-KISS gene (2016) J Exp Bot, 67, pp. 2127-2138
  • Lee, H.-S., Karunanandaa, B., McCubbin, A., Gilroy, S., Kao, T.-H., PRK1, a receptor-like kinase of Petunia inflata, is essential for postmeiotic development of pollen (1996) Plant J, 9, pp. 613-624
  • 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 (1998) Plant Cell, 10, pp. 319-330
  • Gui, C.P., Dong, X., Liu, H.K., Huang, W.J., Zhang, D., Wang, S.J., Barberini, M.L., McCormick, S., Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbing mode (2014) Plant Cell, 26, pp. 3538-3555
  • Zhang, D., Wengier, D., Shuai, B., Gui, C.P., Muschietti, J., McCormick, S., Tang, W.H., The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth (2008) Plant Physiol, 148, pp. 1368-1379
  • Salem, T., Mazzella, A., Barberini, M.L., Wengier, D., Motillo, V., Parisi, G., Muschietti, J., Mutations in two putative phosphorylation motifs in the tomato pollen receptor kinase LePRK2 show antagonistic effects on pollen tube length (2011) J Biol Chem, 286, pp. 4882-4891
  • Wengier, D., Valsecchi, I., Cabanas, M.L., Tang, W.H., McCormick, S., Muschietti, J., The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract (2003) Proc Natl Acad Sci U S A, 100, pp. 6860-6865
  • Tang, W., Ezcurra, I., Muschietti, J., McCormick, S., A cysteine-rich extracellular protein, LAT52, interacts with the extracellular domain of the pollen receptor kinase LePRK2 (2002) Plant Cell, 14, pp. 2277-2287
  • Tang, W., Kelley, D., Ezcurra, I., Cotter, R., McCormick, S., LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro (2004) Plant J, 39, pp. 343-353
  • Wengier, D.L., Mazzella, M.A., Salem, T.M., McCormick, S., Muschietti, J.P., STIL, a peculiar molecule from styles, specifically dephosphorylates the pollen receptor kinase LePRK2 and stimulates pollen tube growth in vitro (2010) BMC Plant Biol, 10, p. 33
  • Zhang, D., Wengier, D., Shuai, B., Gui, C.-P., Muschietti, J., McCormick, S., Tang, W.-H., The pollen receptor kinase LePRK2 mediates growth-promoting signals and positively regulates pollen germination and tube growth (2008) Plant Physiol, 148, pp. 1368-1379
  • Kaothien, P., Ok, S.H., Shuai, B., Wengier, D., Cotter, R., Kelley, D., Kiriakopolos, S., McCormick, S., Kinase partner protein interacts with the LePRK1 and LePRK2 receptor kinases and plays a role in polarized pollen tube growth (2005) Plant J, 42, pp. 492-503
  • Zhang, Y., McCormick, S., A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana (2007) Proc Natl Acad Sci U S A, 104, pp. 18830-18835
  • Chang, F., Gu, Y., Ma, H., Yang, Z., AtPRK2 promotes ROP1 activation via RopGEFs in the control of polarized pollen tube growth (2013) Mol Plant, 6, pp. 1187-1201
  • Boisson-Dernier, A., Kessler, S.A., Grossniklaus, U., The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals (2011) J Exp Bot, 62, pp. 1581-1591
  • Huck, N., Moore, J.M., Federer, M., Grossniklaus, U., The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception (2003) Development, 130, pp. 2149-2159
  • Boisson-Dernier, A., Lituiev, D.S., Nestorova, A., Franck, C.M., Thirugnanarajah, S., Grossniklaus, U., ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases (2013) PLoS Biol, 11, p. e1001719. , This paper shows that overexpression of ANXR1/2 inhibits pollen tube growth because exocytosis is overstimulated and cell wall material at the tip area is accumulated. It also shows that ANXRs function upstream of NADPH oxidases
  • Duan, Q., Kita, D., Johnson, E.A., Aggarwal, M., Gates, L., Wu, H.M., Cheung, A.Y., Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis (2014) Nat Commun, 5, p. 3129
  • Schallus, T., Jaeckh, C., Feher, K., Palma, A.S., Liu, Y., Simpson, J.C., Mackeen, M., Feizi, T., Malectin: a novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation (2008) Mol Biol Cell, 19, pp. 3404-3414
  • Haruta, M., Sabat, G., Stecker, K., Minkoff, B.B., Sussman, M.R., A peptide hormone and its receptor protein kinase regulate plant cell expansion (2014) Science, 343, pp. 408-411
  • Stegmann, M., Monaghan, J., Smakowska-Luzan, E., Rovenich, H., Lehner, A., Holton, N., Belkhadir, Y., Zipfel, C., The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling (2017) Science, 355, pp. 287-289. , This paper reports that the RALFL peptide, RALFL23 restrains immune response through the inhibitory association with FER who promotes the formation of the active FLS2/EFR-BAK1 complex
  • Bai, L., Zhang, G., Zhou, Y., Zhang, Z., Wang, W., Du, Y., Wu, Z., Song, C.-P., Plasma membrane-associated proline-rich extensin-like receptor kinase 4, a novel regulator of Ca2+ signalling, is required for abscisic acid responses in Arabidopsis thaliana (2009) Plant J, 1, pp. 314-327
  • Kohorn, B.D., Cell wall-associated kinases and pectin perception (2016) J Exp Bot, 67, pp. 489-494
  • Kanaoka, M.M., Higashiyama, T., Peptide signaling in pollen tube guidance (2015) Curr Opin Plant Biol, 28, pp. 127-136
  • Liu, J., Zhong, S., Guo, X., Hao, L., Wei, X., Huang, Q., Hou, Y., Gu, H., Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis (2013) Curr Biol, 23, pp. 993-998
  • Mayank, P., Grossman, J., Wuest, S., Boisson-Dernier, A., Roschitzki, B., Nanni, P., Nuhse, T., Grossniklaus, U., Characterization of the phosphoproteome of mature Arabidopsis pollen (2012) Plant J, 72, pp. 89-101. , This was the first phosphoproteomic study of mature Arabidopsis pollen grains. In this study 598 pollen phosphoproteins were identified
  • Jiang, J., Zhang, C., Wang, X., Ligand perception, activation, and early signaling of plant steroid receptor brassinosteroid insensitive 1 (2013) J Integr Plant Biol, 55, pp. 1198-1211
  • Chatr-aryamontri, A., Breitkreutz, B.J., Heinicke, S., Boucher, L., Winter, A., Stark, C., Nixon, J., O'Donnell, L., The BioGRID interaction database: 2013 update (2013) Nucleic Acids Res, 41, pp. D816-D823
  • Geisler-Lee, J., O'Toole, N., Ammar, R., Provart, N.J., Millar aH, Geisler, M., A predicted interactome for Arabidopsis (2007) Plant Physiol, 145, pp. 317-329
  • Hermjakob, H., Montecchi-Palazzi, L., Lewington, C., Mudali, S., Kerrien, S., Orchard, S., Vingron, M., Valencia, A., IntAct: an open source molecular interaction database (2004) Nucleic Acids Res, 32, pp. D452-D455
  • Lalonde, S., Sero, A., Pratelli, R., Pilot, G., Chen, J., Sardi, M.I., Parsa, S.A., Stein, E.V., A membrane protein/signaling protein interaction network for Arabidopsis version AMPv2 (2010) Front Physiol, 1, p. 24
  • Jones, A.M., Xuan, Y., Xu, M., Wang, R.S., Ho, C.H., Lalonde, S., You, C.H., Smith-Valle, E., Border control — a membrane-linked interactome of Arabidopsis (2014) Science, 344, pp. 711-716
  • Qin, Y., Leydon, A.R., Manziello, A., Pandey, R., Mount, D., Denic, S., Vasic, B., Palanivelu, R., Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil (2009) PLoS Genet, 5, p. e1000621. , This article describes for the first time the pollen genes expressed during pollen tube growth through stigma and style tissues
  • Roschzttardtz, H., Séguéla-Arnaud, M., Briat, J.-F., Vert, G., Curie, C., The FRD3 citrate effluxer promotes iron nutrition between symplastically disconnected tissues throughout Arabidopsis development (2011) Plant Cell, 23, pp. 2725-2737
  • Cakmak, I., Possible roles of zinc in protecting plant cells from damage by reactive oxygen species (2000) New Phytol, 146, pp. 185-205
  • O'Brien, J.A., Daudi, A., Butt, V.S., Paul Bolwell, G., Reactive oxygen species and their role in plant defence and cell wall metabolism (2012) Planta, 236, pp. 765-779
  • Rogers, E.E., Guerinot, M.L., FRD3, a member of the multidrug and toxin efflux family, controls iron deficiency responses in Arabidopsis (2002) Plant Cell, 14, pp. 1787-1799
  • Stonebloom, S., Ebert, B., Xiong, G., Pattathil, S., Birdseye, D., Lao, J., Pauly, M., Scheller, H.V., A DUF-246 family glycosyltransferase-like gene affects male fertility and the biosynthesis of pectic arabinogalactans (2016) BMC Plant Biol, 16, p. 90. , This report reveals that a pectic arabinogalactan synthesis-related enzyme (PAGR) is essential for pollen tube growth
  • Wang, J., Ding, Y., Wang, J., Hillmer, S., Miao, Y., Lo, S.W., Wang, X., Jiang, L., EXPO, an exocyst-positive organelle distinct from multivesicular endosomes and autophagosomes, mediates cytosol to cell wall exocytosis in Arabidopsis and tobacco cells (2010) Plant Cell, 22, pp. 4009-4030
  • Poulsen, C.P., Dilokpimol, A., Mouille, G., Burow, M., Geshi, N., Arabinogalactan glycosyltransferases target to a unique subcellular compartment that may function in unconventional secretion in plants (2014) Traffic (Copenhagen, Denmark), 15, pp. 1219-1234
  • Cole, R.A., Synek, L., Zarsky, V., Fowler, J.E., SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth (2005) Plant Physiol, 138, pp. 2005-2018
  • Hála, M., Cole, R., Synek, L., Drdová, E., Pečenková, T., Nordheim, A., Lamkemeyer, T., Fowler, J.E., An exocyst complex functions in plant cell growth in Arabidopsis and tobacco (2008) Plant Cell, 20, pp. 1330-1345
  • Wrzaczek, M., Brosché, M., Kollist, H., Kangasjärvi, J., Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS (2009) Proc Natl Acad Sci U S A, 106, pp. 5412-5417
  • Wrzaczek, M., Vainonen, J.P., Stael, S., Tsiatsiani, L., Help-Rinta-Rahko, H., Gauthier, A., Kaufholdt, D., Staes, A., GRIM REAPER peptide binds to receptor kinase PRK5 to trigger cell death in Arabidopsis (2015) EMBO J, 34, pp. 55-66
  • Gelhaye, E., Rouhier, N., Navrot, N., Jacquot, J.P., The plant thioredoxin system (2005) Cell Mol Life Sci, 62, pp. 24-35
  • Laloi, C., Mestres-Ortega, D., Marco, Y., Meyer, Y., Reichheld, J.-P., The Arabidopsis cytosolic thioredoxin h5 gene induction by oxidative stress and its W-Box-mediated response to pathogen elicitor (2004) Plant Physiol, 134, pp. 1006-1016
  • Riondet, C., Desouris, J.P., Montoya, J.G., Chartier, Y., Meyer, Y., Reichheld, J.-P., A dicotyledon-specific glutaredoxin GRXC1 family with dimer-dependent redox regulation is functionally redundant with GRXC2 (2012) Plant Cell Environ, 35, pp. 360-373
  • Reichheld, J.-P., Khafif, M., Riondet, C., Droux, M., Bonnard, G., Meyer, Y., Inactivation of thioredoxin reductases reveals a complex interplay between thioredoxin and glutathione pathways in Arabidopsis development (2007) Plant Cell, 19, pp. 1851-1865
  • Marty, L., Siala, W., Schwarzländer, M., Fricker, M.D., Wirtz, M., Sweetlove, L.J., Meyer, Y., Hell, R., The NADPH-dependent thioredoxin system constitutes a functional backup for cytosolic glutathione reductase in Arabidopsis (2009) Proc Natl Acad Sci U S A, 106, pp. 9109-9114
  • Nekrasov, V., Ludwig, A.A., Jones, J.D.G., CITRX thioredoxin is a putative adaptor protein connecting Cf-9 and the ACIK1 protein kinase during the Cf-9/Avr9-induced defence response (2006) FEBS Lett, 580, pp. 4236-4241
  • Rivas, S., Rougon-Cardoso, A., Smoker, M., Schauser, L., Yoshioka, H., Jones, J.D.G., CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence (2004) EMBO J, 23, pp. 2156-2165
  • Ichimura, K., Shinozaki, K., Tena, G., Sheen, J., Henry, Y., Champion, A., Kreis, M., Wilson, C., Mitogen-activated protein kinase cascades in plants: a new nomenclature (2002) Trends Plant Sci, 7, pp. 301-308
  • Guan, Y., Lu, J., Xu, J., McClure, B., Zhang, S., Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis (2014) Plant Physiol, 165, pp. 528-533. , Here, evidence is provided that pollen MPK3 and MPK6 are involved in mediating the guidance response during fertilization. Pollen of the double mutant mpk3 mpk6 has reduced transmission
  • Furlan, G., Nakagami, H., Eschen-Lippold, L., Jiang, X., Majovsky, P., Kowarschik, K., Hoehenwarter, W., Trujillo, M., Changes in PUB22 ubiquitination modes triggered by MITOGEN-ACTIVATED PROTEIN KINASE3 dampen the immune response (2017) Plant Cell, 29, pp. 726-745
  • Stegmann, M., Anderson, R.G., Ichimura, K., Pecenkova, T., Reuter, P., Žárský, V., McDowell, J.M., Trujillo, M., The ubiquitin ligase PUB22 targets a subunit of the exocyst complex required for PAMP-triggered responses in Arabidopsis (2012) Plant Cell, 24, pp. 4703-4716
  • Deeks, M.J., Calcutt, J.R., Ingle, E.K.S., Hawkins, T.J., Chapman, S., Richardson, A.C., Mentlak, D.A., Smertenko, A.P., A superfamily of actin-binding proteins at the actin-membrane nexus of higher plants (2012) Curr Biol, 22, pp. 1595-1600
  • Skirpan, A.L., McCubbin, A.G., Ishimizu, T., Wang, X., Hu, Y., Dowd, P.E., Ma, H., Kao, T., Isolation and characterization of kinase interacting protein 1, a pollen protein that interacts with the kinase domain of PRK1, a receptor-like kinase of petunia (2001) Plant Physiol, 126, pp. 1480-1492
  • Lozano-Juste, J., León, J., Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis (2010) Plant Physiol, 152, pp. 891-903
  • Evans, A.R., Hall, D., Pritchard, J., Newbury, H.J., The roles of the cation transporters CHX21 and CHX23 in the development of Arabidopsis thaliana (2012) J Exp Bot, 63, pp. 59-67
  • Lu, Y., Chanroj, S., Zulkifli, L., Johnson, M.A., Uozumi, N., Cheung, A., Sze, H., Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis (2011) Plant Cell, 23, pp. 81-93
  • Zhang, Z., Mao, Y., Ha, S., Liu, W., Botella, J.R., Zhu, J.K., A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis (2016) Plant Cell Rep, 35, pp. 1519-1533
  • Lease, K.A., Walker, J.C., The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics (2006) Plant Physiol, 142, pp. 831-838
  • Butenko, M.A., Wildhagen, M., Albert, M., Jehle, A., Kalbacher, H., Aalen, R.B., Felix, G., Tools and strategies to match peptide-ligand receptor pairs (2014) Plant Cell, 26, pp. 1838-1847
  • Prado, A.M., Porterfield, D.M., Feijo, J.A., Nitric oxide is involved in growth regulation and re-orientation of pollen tubes (2004) Development, 131, pp. 2707-2714
  • Honys, D., Twell, D., Comparative analysis of the Arabidopsis pollen transcriptome (2003) Plant Physiol, 132, pp. 640-652

Citas:

---------- APA ----------
Muschietti, J.P. & Wengier, D.L. (2018) . How many receptor-like kinases are required to operate a pollen tube. Current Opinion in Plant Biology, 41, 73-82.
http://dx.doi.org/10.1016/j.pbi.2017.09.008
---------- CHICAGO ----------
Muschietti, J.P., Wengier, D.L. "How many receptor-like kinases are required to operate a pollen tube" . Current Opinion in Plant Biology 41 (2018) : 73-82.
http://dx.doi.org/10.1016/j.pbi.2017.09.008
---------- MLA ----------
Muschietti, J.P., Wengier, D.L. "How many receptor-like kinases are required to operate a pollen tube" . Current Opinion in Plant Biology, vol. 41, 2018, pp. 73-82.
http://dx.doi.org/10.1016/j.pbi.2017.09.008
---------- VANCOUVER ----------
Muschietti, J.P., Wengier, D.L. How many receptor-like kinases are required to operate a pollen tube. Curr. Opin. Plant Biol. 2018;41:73-82.
http://dx.doi.org/10.1016/j.pbi.2017.09.008