Arabidopsis thaliana calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca2+ concentration

Plant Molecular Biology - Tập 86 - Trang 225-236 - 2014
Xue Yang1,2, Shuang-Shuang Wang1, Mei Wang1, Zhu Qiao1, Chan-Chan Bao3, Wei Zhang1
1Key Laboratory of Plant Cell Engineering and Germplasm Innovation, Ministry of Education, School of Life Science, Shandong University, Jinan, China
2College of Technological Gardening, Shandong Yingcai University, Jinan, China
3The Microscopy Characterization Platform, Shandong University, Jinan, China

Tóm tắt

Cytosolic free calcium ([Ca2+]cyt), which is essential during pollen germination and pollen tube growth, can be sensed by calmodulin-like proteins (CMLs). The Arabidopsis thaliana genome encodes over 50 CMLs, the physiological role(s) of most of which are unknown. Here we show that the gene AtCML24 acts as a regulator of pollen germination and pollen tube extension, since the pollen produced by loss-of-function mutants germinated less rapidly than that of wild-type (WT) plants, the rate of pollen tube extension was slower, and the final length of the pollen tube was shorter. The [Ca2+]cyt within germinated pollen and extending pollen tubes produced by the cml24 mutant were higher than their equivalents in WT plants, and pollen tube extension was less sensitive to changes in external [K+] and [Ca2+]. The pollen and pollen tubes produced by cml24 mutants were characterized by a disorganized actin cytoskeleton and lowered sensitivity to the action of latrunculin B. The observations support an interaction between CML24 and [Ca2+]cyt and an involvement of CML24 in actin organization, thereby affecting pollen germination and pollen tube elongation.

Tài liệu tham khảo

Azimzadeh J, Nacry P, Christodoulidou A, Drevensek S, Camilleri C, Amiour N, Parcy F, Pastuglia M, Bouchez D (2008) Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin. Plant Cell 20(8):2146–2159 Bashirullah A, Cooperstock RL, Lipshitz HD (2001) Spatial and temporal control of RNA stability. Proc Natl Acad Sci USA 98:7025–7028 Batistic O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820(8):1283–1293 Boavida LC, McCormick S (2007) TECHNICAL ADVANCE: Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52(3):570–582 Cardenas L, Lovy-Wheeler A, Kunkel JG, Hepler PK (2008) Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization. Plant Physiol 146(4):1611–1621 Chebli Y, Kroeger J, Geitmann A (2013) Transport logistics in pollen tubes. Mol Plant 6(4):1037–1052 Chen N, Qu X, Wu Y, Huang S (2009) Regulation of actin dynamics in pollen tubes: control of actin polymer level. J Integr Plant Biol 51(8):740–750 Cheung AY, Wu HM (2008) Structural and signaling networks for the polar cell growth machinery in pollen tubes. Annu Rev Plant Biol 59:547–572 Cheung AY, Duan QH, Costa SS, de Graaf BH, Di Stilio VS, Feijo J, Wu HM (2008) The dynamic pollen tube cytoskeleton: live cell studies using actin-binding and microtubule-binding reporter proteins. Mol Plant 1(4):686–702 Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743 DeFalco TA, Bender KW, Snedden WA (2010) Breaking the code: Ca2+ sensors in plant signalling. Biochem J 425(1):27–40 Delk NA, Johnson KA, Chowdhury NI, Braam J (2005) CML24, regulated in expression by diverse stimuli, encodes a potential Ca2+ sensor that functions in responses to abscisic acid, daylength, and ion stress. Plant Physiol 139(1):240–253 Dong H, Pei W, Haiyun R (2012) Actin fringe is correlated with tip growth velocity of pollen tubes. Mol Plant 5(5):1160–1162 Fan LM, Wang YF, Wang H, Wu WH (2001) In vitro Arabidopsis pollen germination and characterization of the inward potassium currents in Arabidopsis pollen grain protoplasts. J Exp Bot 52(361):1603–1614 Franklin-Tong N (2010) Plant fertilization: bursting pollen tubes! Curr Biol 20(16):R681–R683 Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin controls tip growth in pollen tubes. J Cell Biol 152(5):1019–1032 Fujiki Y, Yoshimoto K, Ohsumi Y (2007) An Arabidopsis homolog of yeast ATG6/VPS30 is essential for pollen germination. Plant Physiol 143(3):1132–1139 Gibbon BC, Kovar DR, Staiger CJ (1999) Latrunculin B has different effects on pollen germination and tube growth. Plant Cell 11(12):2349–2363 Gu Y, Fu Y, Dowd P, Li S, Vernoud V, Gilroy S, Yang Z (2005) A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J Cell Biol 169(1):127–138 Harrison-Lowe NJ, Olsen LJ (2008) Autophagy protein 6 (ATG6) is required for pollen germination in Arabidopsis thaliana. Autophagy 4(3):339 Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17:159–187 Holdaway-Clarke TL, Feijo JA, Hackett GR, Kunkel JG, Hepler PK (1997) Pollen tube growth and the intracellular cytosolic calcium gradient oscillate in phase while extracellular calcium influx is delayed. Plant Cell 9(11):1999–2010 Hwang JU, Gu Y, Lee YJ, Yang Z (2005) Oscillatory ROP GTPase activation leads the oscillatory polarized growth of pollen tubes. Mol Biol Cell 16(11):5385–5399 Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13(10):2191–2209 Iwano M, Shiba H, Miwa T, Che FS, Takayama S, Nagai T, Miyawaki A, Isogai A (2004) Ca2+ dynamics in a pollen grain and papilla cell during pollination of Arabidopsis. Plant Physiol 136(3):3562–3571 Jaffe LA, Weisenseel MH, Jaffe LF (1975) Calcium accumulations within the growing tips of pollen tubes. J Cell Biol 67(2PT.1):488–492 Konrad KR, Wudick MM, Feijó JA (2011) Calcium regulation of tip growth: new genes for old mechanisms. Curr Opin Plant Biol 14(6):721–730 Landoni M, De Francesco A, Galbiati M, Tonelli C (2010) A loss-of-function mutation in calmodulin2 gene affects pollen germination in Arabidopsis thaliana. Plant Mol Biol 74(3):235–247 Lazzaro MD, Cardenas L, Bhatt AP, Justus CD, Phillips MS, Holdaway-Clarke TL, Hepler PK (2005) Calcium gradients in conifer pollen tubes; dynamic properties differ from those seen in angiosperms. J Exp Bot 56(420):2619–2628 Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237 Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402–408 Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221(1):95–104 Ma W, Smigel A, Tsai YC, Braam J, Berkowitz GA (2008) Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148(2):818–828 McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159(3):585–598 Mouline K, Very AA, Gaymard F, Boucherez J, Pilot G, Devic M, Bouchez D, Thibaud JB, Sentenac H (2002) Pollen tube development and competitive ability are impaired by disruption of a Shaker K(+) channel in Arabidopsis. Genes Dev 16(3):339–350 Obermeyer G, Weisenseel MH (1991) Calcium channel blocker and calmodulin antagonists affect the gradient of free calcium ions in lily pollen tubes. Eur J Cell Biol 56(2):319–327 Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581(12):2325–2336 Picton JM, Steer MW (1983) Membrane recycling and the control of secretory activity in pollen tubes. J Cell Sci 63:303–310 Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174(1):160–173 Qu H, Jiang X, Shi Z, Liu L, Zhang S (2012) Fast loading ester fluorescent Ca2+ and pH indicators into pollen of Pyrus pyrifolia. J Plant Res 125(1):185–195 Ren H, Xiang Y (2007) The function of actin-binding proteins in pollen tube growth. Protoplasma 230(3–4):171–182 Schiefelbein J, Galway M, Masucci J, Ford S (1993) Pollen tube and root-hair tip growth is disrupted in a mutant of Arabidopsis thaliana. Plant Physiol 103(3):979–985 Staiger CJ, Poulter NS, Henty JL, Franklin-Tong VE, Blanchoin L (2010) Regulation of actin dynamics by actin-binding proteins in pollen. J Exp Bot 61(7):1969–1986 Taylor LP, Hepler PK (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48:461–491 Tsai YC, Delk NA, Chowdhury NI, Braam J (2007) Arabidopsis potential calcium sensors regulate nitric oxide levels and the transition to flowering. Plant Signal Behav 2(6):446–454 Tsai YC, Koo Y, Delk NA, Gehl B, Braam J (2013) Calmodulin-related CML24 interacts with ATG4b and affects autophagy progression in Arabidopsis. Plant J 73(2):325–335 Vidali L, Rounds CM, Hepler PK, Bezanilla M (2009) Lifeact-mEGFP reveals a dynamic apical F-actin network in tip growing plant cells. PLoS One 4(5):e5744 Wang YF, Fan LM, Zhang WZ, Zhang W, Wu WH (2004) Ca2+-permeable channels in the plasma membrane of Arabidopsis pollen are regulated by actin microfilaments. Plant Physiol 136(4):3892–3904 Winter J, Roepcke S, Krause S, Müller E-C, Otto A, Vingron M, Schweiger S (2008) Comparative 3′UTR analysis allows identification of regulatory clusters that drive Eph/ephrin expression in cancer cell lines. PLoS One 3(7):e2780 Wu Y, Yan J, Zhang R, Qu X, Ren S, Chen N, Huang S (2010) Arabidopsis FIMBRIN5, an actin bundling factor, is required for pollen germination and pollen tube growth. Plant Cell 22(11):3745–3763 Xiang Y, Huang X, Wang T, Zhang Y, Liu Q, Hussey PJ, Ren H (2007) ACTIN BINDING PROTEIN 29 from Lilium pollen plays an important role in dynamic actin remodeling. Plant Cell 19(6):1930–1946 Zhang W, Fan LM, Wu WH (2007) Osmo-sensitive and stretch-activated calcium-permeable channels in Vicia faba guard cells are regulated by actin dynamics. Plant Physiol 143(3):1140–1151 Zhang H, Qu X, Bao C, Khurana P, Wang Q, Xie Y, Zheng Y, Chen N, Blanchoin L, Staiger CJ, Huang S (2010) Arabidopsis VILLIN5, an actin filament bundling and severing protein, is necessary for normal pollen tube growth. Plant Cell 22(8):2749–2767 Zhao LN, Shen LK, Zhang WZ, Zhang W, Wang Y, Wu WH (2013) Ca2+-dependent protein kinase11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tubes. Plant Cell 25:649–661