Role of CMLs in regulating the competition of plant pollen pollination

Gao Shumin; Yang Muhan; Zhu Yuanyuan; Zhou Yan

doi:10.13332/j.1000-1522.20180375

Journal of Beijing Forestry University > 2019 > 41(3): 143-150. > DOI: 10.13332/j.1000-1522.20180375

Gao Shumin, Yang Muhan, Zhu Yuanyuan, Zhou Yan. Role of CMLs in regulating the competition of plant pollen pollination[J]. Journal of Beijing Forestry University, 2019, 41(3): 143-150. DOI: 10.13332/j.1000-1522.20180375

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Role of CMLs in regulating the competition of plant pollen pollination

Gao Shumin^1,,
Yang Muhan^1,2,
Zhu Yuanyuan^1,2,
Zhou Yan^1,2, ,

1.
College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing 100083, China
2.
Beijing Institute of Landscape Architecture; Beijing Key Laboratory of Greening Plants Breeding, Beijing 100102, China

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Received Date: November 20, 2018
Revised Date: January 02, 2019
Available Online: March 31, 2019
Published Date: February 28, 2019

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Abstract

Abstract

ObjectivePollen germination and pollen tube growth play a critical role in reproductive process of flowering plants. Pollen germination and pollen tube growth is regulated directly or indirectly by many factors, such as calmodulin-like proteins (CMLs). However, very little research has focused on the function of CMLs till now. The aim of this paper is to reveal the role of CML proteins in the competitive advantage of pollen, and to provide a theoretical foundation for further exploring the molecular mechanism of CMLs in plant pollen competitive advantage.
MethodThis paper comprehensively summarizes the structure, expression level, cell localization and mechanisms of CMLs proteins involved in the regulation of pollen germination and pollen tube growth, and analyzes the pollen competition phenomena in different plants.
ResultThere were about four conserved EF-hand domains in CMLs. When CMLs bind to Ca²⁺, its conformation changes enhanced its binding ability to downstream receptor proteins, and initiated Ca²⁺ dependent cascade signal amplification effect, which resulted in changes in Ca²⁺ concentration in pollen tube and influenced the formation of Ca²⁺ concentration gradient from germination aperture to the top of pollen tube, thus regulating the normal growth of pollen tube. The expression of CML proteins can also affect the concentration of Mg²⁺, NO and the binding of Ca²⁺ to EF-hand domains and the orientation of pollen tube growth. Different CML proteins had different physiological functions. Among them, CML proteins involved in pollen germination and pollen tube growth were mainly expressed in plant floral organs. During fertilization of some flowering plants, different ploidy pollens may have different germination rates and growth rates due to differences in genome size or nutrient content.
ConclusionCMLs proteins may affect the process of pollen germination in vivo by differentially expressing in different ploidy pollens, and make them show competitive advantage in a certain period of time.
- CMLs,
- pollen germination,
- pollen tube growth,
- competitive advantage,
- regulating

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References (62)

References

[1]	DeFalco T A, Bender K W, Snedden W A. Breaking the code: Ca²⁺ sensors in plant signaling[J]. Biochemical Journal, 2010, 425(1): 27−40. doi: 10.1042/BJ20091147
[2]	Bender K W, Snedden W A. Calmodulin-related proteins step out from the shadow of their namesake[J]. Plant Physiology, 2013, 163(2): 486−495. doi: 10.1104/pp.113.221069
[3]	Abbas N, Maurya J P, Senapati D, et al. Arabidopsis CAM7 and HY5 physically interact and directly bind to the HY5 promoter to regulate its expression and thereby promote photomorxphogenesis[J]. The Plant Cell, 2014, 26(3): 1036−1052. doi: 10.1105/tpc.113.122515
[4]	Chen C, Duanmu H Z, Zhu D, et al. Bioinformatics analysis of GmCML genes in soybean genome[J]. Soybean Science, 2015, 13(7): 427−435.
[5]	Perochon A, Aldon D, Galaud J P, et al. Calmodulin and calmodulin-like proteins in plant calcium signaling[J]. Biochimie, 2011, 93(12): 2048−2053. doi: 10.1016/j.biochi.2011.07.012
[6]	Song M, Xu J Q, Sun Z J, et al. Molecular cloning and expression analysis of cam-like protein genes (bocml49) from cabbage (Brassica oleracea L. var. capitata)[J]. Acta Agronomica Sinica, 2012, 38(12): 2162−2169.
[7]	La V V, Trande M, D’Onofrio M, et al. Binding of calcium and target peptide to calmodulin-like protein CML19, the centrin 2 of Arabidopsis thaliana[J]. International Journal of Biological Macromolecules, 2018, 108: 1289−1299. doi: 10.1016/j.ijbiomac.2017.11.044
[8]	Zeng H Q, Zhang Y X, Zhang X J, et al. Analysis of EF-hand proteins in soybean genome suggests their potential roles in environmental and nutritional stress signaling[J]. Frontiers in Plant Science, 2017, 8: 877. doi: 10.3389/fpls.2017.00877
[9]	Mccormack E, Braam J. Calmodulins and related potential calcium sensors of Arabidopsis[J]. New Phytologist, 2003, 159(3): 585−598. doi: 10.1046/j.1469-8137.2003.00845.x
[10]	Ogunrinde A, Munro K, Davidson A, et al. Arabidopsis calmodulin-like proteins, CML15 and CML16 possess biochemical properties distinct from calmodulin and show non-overlapping tissue expression patterns[J]. Frontiers in Plant Science, 2017, 8: 2175. doi: 10.3389/fpls.2017.02175
[11]	Finn B E, Evenäs J, Drakenberg T, et al. Calcium-induced structural changes and domain autonomy in calmodulin[J]. Nat Struct Biol, 1995, 2(9): 777−783. doi: 10.1038/nsb0995-777
[12]	Ikura M, Tanaka T, Zhang Q M. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin[J]. Nature Structural Biology, 1995, 2(9): 758−767. doi: 10.1038/nsb0995-758
[13]	Chigri F, Flosdorff S, Pilz S, et al. The Arabidopsis calmodulin-like proteins AtCML30 and AtCML3 are targeted to mitochondria and peroxisomes, respectively[J]. Plant Molecular Biology, 2012, 78(3): 211−222. doi: 10.1007/s11103-011-9856-z
[14]	Yang T B, Poovaiah B W. Calcium/calmodulin-mediated signal network in plants[J]. Trends in Plant Science, 2003, 8(10): 505−512. doi: 10.1016/j.tplants.2003.09.004
[15]	Boonburapong B, Buaboocha T. Genome-wide identification and analyses of the rice calmodulin and related potential calcium sensor proteins[J]. Bmc Plant Biology, 2007, 7(1): 4−10. doi: 10.1186/1471-2229-7-4
[16]	Gong M, Yang Z H, Cao Z X. Involvement of calmodulin in pollen germination and pollen tube growth[J]. Acta Phytophisiologica Sinica, 1994(3): 240−248.
[17]	Ma L G, Fan Q S, Yu Z Q, et al. Does aluminum inhibit pollen germination via extracellular calmodulin?[J]. Plant & Cell Physiology, 2000, 41(3): 372−376.
[18]	Vanderbeld B, Snedden W A. Developmental and stimulus-induced expression patterns of Arabidopsis calmodulin-like genes CML37, CML38 and CML39[J]. Plant Molecular Biology, 2007, 64(6): 683−697. doi: 10.1007/s11103-007-9189-0
[19]	李娜. 拟南芥钙调素类似蛋白CML24调控铝抑制根伸长的机制研究[D]. 济南: 山东大学, 2015. Li N. Calmodulin like protein (CML24) medicates Al-induced root growth inhibition of Arabidopsis[D]. Jinan: Shangdong University, 2015.
[20]	Zhu X Y, Robe E, Jomat L, et al. CML8, an Arabidopsis calmodulin-like protein, plays a role in pseudomonas syringae plant immunity[J]. Plant & Cell Physiology, 2017, 58(2): 307−319.
[21]	Aumnart C, Kampon L, Srivilai P, et al. Expression analysis of calmodulin and calmodulin-like genes from rice, Oryza sativa L.[J]. Bmc Research Notes, 2012, 5(1): 625−625. doi: 10.1186/1756-0500-5-625
[22]	Wang S S, Diao W Z, Yang X, et al. Arabidopsis thaliana CML25 mediates the Ca²⁺ regulation of K⁺ transmembrane trafficking during pollen germination and tube elongation[J]. Plant Cell & Environment, 2015, 38(11): 2372−2386.
[23]	Yang X, Wang S S, Wang M, et al. Arabidopsis thaliana, calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca²⁺, concentration[J]. Plant Molecular Biology, 2014, 86(3): 225−236. doi: 10.1007/s11103-014-0220-y
[24]	Lin W D, Liao Y Y, Yang T J, et al. Coexpression-based clustering of Arabidopsis root genes predicts functional modules in early phosphate deficiency signaling[J]. Plant Signaling & Behavior, 2011, 155(5): 1383−1402.
[25]	Bender K W, Rosenbaum D M, Vanderbeld B, et al. The Arabidopsis calmodulin-like protein, CML39, functions during early seedling establishment[J]. Plant Journal, 2013, 76(4): 634−647. doi: 10.1111/tpj.2013.76.issue-4
[26]	Magnan F, Ranty B M, Sotta B, et al. Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid[J]. Plant Journal, 2010, 56(4): 575−589.
[27]	Azimzadeh J, Nacry P, Christodoulidou A, et al. Arabidopsis TONNEAU1 proteins are essential for preprophase band formation and interact with centrin[J]. The Plant Cell, 2008, 20(8): 2146−2159. doi: 10.1105/tpc.107.056812
[28]	Dobney S, Chiasson D, Lam P, et al. The calmodulin-related calcium sensor cml42 plays a role in trichome branching[J]. Journal of Biological Chemistry, 2009, 284(46): 31647−31657. doi: 10.1074/jbc.M109.056770
[29]	Pannell J R, Labouche A M. The incidence and selection of multiple mating in plants[J]. Philosophical Transactions of the Royal Society of London, 2013, 368(1613): 20120051. doi: 10.1098/rstb.2012.0051
[30]	Marshall D L, Ellstrand N C. Proximal causes of multiple paternity in wild radish, Raphanus sativus[J]. American Naturalist, 1985, 126(5): 596−605. doi: 10.1086/284441
[31]	Burkhardt A, Internicola A, Bernasconi G. Effects of pollination timing on seed paternity and seed mass in Silene latifolia (Caryophyllaceae)[J]. Annals of Botany, 2009, 104(4): 767−773. doi: 10.1093/aob/mcp154
[32]	Snow A A, Spira T P. Pollen vigour and the potential for sexual selection in plants[J]. Nature, 1991, 352(6338): 796−797. doi: 10.1038/352796a0
[33]	Pasonen H L, Pulkkinen P, Kapyla M, et al. Pollen-tube growth rate and seed-siring success among Betula pendula clones[J]. New Phytologist, 2010, 143(2): 243−251.
[34]	Jolivet C, Bernasconi G. Within/between population crosses reveal genetic basis for siring success in Silene latifolia, (Caryophyllaceae)[J]. Journal of Evolutionary Biology, 2007, 20(4): 1361−1374. doi: 10.1111/jeb.2007.20.issue-4
[35]	Mccallum B, Chang S M. Pollen competition in style: effects of pollen size on siring success in the hermaphroditic common morning glory, ipomoea purpurea[J]. American Journal of Botany, 2016, 103(3): 460. doi: 10.3732/ajb.1500211
[36]	赖杭桂. 木薯2n配子途径诱导多倍体的研究[D]. 海口: 海南大学, 2014. Lai H G. Research on induction of cassava polyploid through 2n gametes[D]. Haikou: Hainan University, 2014.
[37]	Kang X Y, Zhu Z T. A study on the 2n pollen vitality and germinant characteristics of white populars[J]. Acta Botanica Yunnanica, 1997, 19(4): 402−406.
[38]	Vanbreukelen E W M, 董延瑜. 快速测定活体马铃薯花柱上2X和X花粉间的竞争[J]. 园艺与种苗, 1984(3):26−27. Vanbreukelen E W M, Dong Y Y. Rapid determination of competition between 2X and X pollen on living potato style[J]. Horticulture & Seed, 1984(3): 26−27.
[39]	Qu D Y, Zhu D W, Ramanna M S, et al. A comparison of progeny from diallel crosses of diploid potato with regard to the frequencies of 2n-pollen grains[J]. Euphytica, 1995, 92(3): 313−320. doi: 10.1007/BF00037114
[40]	Liu X. Investigation of ploidy level and embryogenesis of progeny from crosses of tetraploid with diploid in Chinese cabbage[J]. British Journal of Haematology, 1996, 27(1): 153−161.
[41]	Wang Y, Zhang W Z, Song L F, et al. Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis[J]. Plant Physiology, 2008, 148(3): 1201−1211. doi: 10.1104/pp.108.126375
[42]	Zhou L, Ying F U, Yang Z. A genome-wide functional characterization of Arabidopsis regulatory calcium sensors in pollen tubes[J]. Journal of Integrative, 2009, 51(8): 751−761.
[43]	Bender K W, Dobney S, Ogunrinde A, et al. The calmodulin-like protein CML43 functions as a salicylic-acid-inducible root-specific Ca²⁺ sensor in Arabidopsis[J]. Biochemical Journal, 2014, 457(1): 127−136. doi: 10.1042/BJ20131080
[44]	Lenartowska M, Rodríguez-García M I, Bednarska E. Calmodulin and calmodulin-like protein are involved in pollen-pistil interaction: immunocytochemical studies on petunia hybrida hort[J]. Acta Biologica Cracoviensia, 2001, 43(2): 117−123.
[45]	Sun Y, Sun D. Signal transduction in pollen germination and tube growth[J]. Acta Botanica Sinica, 2001, 43(12): 1211−1217.
[46]	Staiger C J, Poulter N S, Henty J L, et al. Regulation of actindynamics by actin-binding proteins in pollen[J]. Journal of Experimental Botany, 2010, 61(7): 1969−1986. doi: 10.1093/jxb/erq012
[47]	Zhang Y, Mccormick S. The regulation of vesicle trafficking by small gtpases and phospholipids during pollen tube growth[J]. Sexual Plant Reproduction, 2010, 23(2): 87−93. doi: 10.1007/s00497-009-0118-z
[48]	Luis Cárdenas, Lovywheeler A, Kunkel J G, et al. Pollen tube growth oscillations and intracellular calcium levels are reversibly modulated by actin polymerization[J]. Plant Physiology, 2008, 146(4): 1611−1621. doi: 10.1104/pp.107.113035
[49]	Dodd A N, Kudla J, Sanders D. The language of calcium signaling[J]. Annual Review of Plant Biology, 2010, 61(1): 593−620. doi: 10.1146/annurev-arplant-070109-104628
[50]	Hepler P K, Kunkel J G, Rounds C M, et al. Calcium entry into pollen tubes[J]. Trends in Plant Science, 2012, 17(1): 32−38. doi: 10.1016/j.tplants.2011.10.007
[51]	Franklintong V E, Drobak B K, Allan A C, et al. Growth of pollen tubes of papaver rhoeas is regulated by a slow-moving calcium wave propagated by inositol 1,4,5-trisphosphate[J]. Plant Cell, 1996, 8(8): 1305−1321. doi: 10.1105/tpc.8.8.1305
[52]	Magnan F, Ranty B M, Sotta B, et al. Mutations in AtCML9, a calmodulin-like protein from Arabidopsis thaliana, alter plant responses to abiotic stress and abscisic acid[J]. Plant Journal, 2010, 56(4): 575−589.
[53]	Li Y Q, Zhang H Q, Pierson E S, et al. Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of lilium longiflorum pollen tubes[J]. Planta, 1996, 200(1): 41−49.
[54]	Mouline K, Véry A A, Gaymard F, et al. Pollen tube development and competitive ability are impaired by disruption of a Shaker K⁺ channel in Arabidopsis[J]. Genes Dev, 2002, 16(3): 339−350. doi: 10.1101/gad.213902
[55]	Waters B M. Moving magnesium in plant cells[J]. New Phytologist, 2011, 190(3): 510−513. doi: 10.1111/nph.2011.190.issue-3
[56]	Ohki S, Ikura M, Zhang M. Identification of Mg²⁺-binding sites and the role of Mg²⁺ on target recognition by calmodulin[J]. Biochemistry, 1997, 36(14): 4309−4316. doi: 10.1021/bi962759m
[57]	Malmendal A, Linse S, Evenäs J, et al. Battle for the EF-hands: magnesium-calcium interference in calmodulin[J]. Biochemistry, 1999, 38(36): 11844−11850. doi: 10.1021/bi9909288
[58]	Clapham D E. Calcium signaling[J]. Cell, 2007, 131(6): 1047−1058. doi: 10.1016/j.cell.2007.11.028
[59]	Gifford J L, Walsh M P, Vogel H J. Structures and metal-ion-binding properties of the Ca²⁺-binding helix-loop-helix EF-hand motifs[J]. Biochemical Journal, 2007, 405(2): 199−221. doi: 10.1042/BJ20070255
[60]	Astegno A, Bonza M C, Vallone R, et al. Arabidopsis calmodulin-like protein CML36 is a calcium (Ca²⁺) sensor that interacts with the plasma membrane Ca²⁺-ATPase Isoform ACA8 and stimulates its activity[J]. Journal of Biological Chemistry, 2017, 292(36): 15049−15061.
[61]	Delk N A, Johnson K A, Chowdhury N I, et al. CML24, regulated in expression by diverse stimuli, encodes a potential Ca²⁺ sensor that functions in responses to abscisic acid, daylength, and ion stress[J]. Plant Physiology, 2005, 139(1): 240−253. doi: 10.1104/pp.105.062612
[62]	杨雪. 拟南芥CML24调控花粉萌发及花粉管生长的功能研究[D]. 济南: 山东大学, 2014 Yang X. Functional study of CML24 in regulating pollen germination and pollen tube growth in Arabiclopsis[D]. Jinan: Shandong University, 2014.

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Role of CMLs in regulating the competition of plant pollen pollination

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