Abstract
Sexual reproductive success is essential for the survival of all higher organisms. As the most prosperous and diverse group of land plants on earth, flowering plants evolved highly sophisticated fertilization mechanisms. To adapt to the terrestrial environment, a tubular structure pollen tube has been evolved to deliver the immobile sperm cells to the egg and central cell enclosed within the ovule. The pollen tube is generated from the vegetative cell of the pollen (male gametophyte), where two sperm cells are hosted. Pollen tube elongation in the maternal tissue and navigation to the ovule require intimate cell–cell interactions between the tube and female tissues. Questions on how the single-celled pollen tube accomplishes such task and how the female tissues accommodate the tube have attracted many plant biologists. Here, we review recent progresses and concepts in understanding the molecular mechanisms governing pollen tube growth and its interactions with the female tissues. We will also discuss the future perspective in this field.
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References
Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–3288
Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719
Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U (2015) Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. PNAS 112:12211–12216
Chae K, Kieslich CA, Morikis D, Kim SC, Lord EM (2009) A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell 21:3902–3914
Chaiwongsar S, Strohm AK, Roe JR, Godiwalla RY, Chan CW (2009) A cyclic nucleotide-gated channel is necessary for optimum fertility in high-calcium environments. New Phytol 183:76–87
Chen YH, Li HJ, Shi DQ, Yuan L, Liu J, Sreenivasan R, Baskar R, Grossniklaus U, Yang WC (2007) The central cell plays a critical role in pollen tube guidance in Arabidopsis. Plant Cell 19:3563–3577
Chen LY, Shi DQ, Zhang WJ, Tang ZS, Liu J, Yang WC (2015) The Arabidopsis alkaline ceramidase TOD1 is a key turgor pressure regulator in plant cells. Nat Commun 6:6030
Cheung AY, Wang H, Wu HM (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82:383–393
Chevalier E, Loubert-Hudon A, Mátton DP (2013) ScRALF3, a secreted RALF-like peptide involved in cell-cell communication between the sporophyte and the female gametophyte in a Solanaceous species. Plant J 73:1019–1033
Covey PA, Subbaiah CC, Parsons RL, Pearce G, Lay FT, Anderson MA, Ryan CA, Bedinger PA (2010) A pollen-specific RALF from tomato that regulates pollen tube elongation. Plant Physiol 153:703–715
Dai XR, Gao XQ, Chen GH, Tang LL, Wang H, Zhang XS (2014) ABNORMAL POLLEN TUBE GUIDANCE1, an endoplasmic reticulum-localized mannosyltransferase homolog of GLYCOSYLPHOSPHATIDYLINOSITOL10 in yeast and PHOSPHATIDYLINOSITOL GLYCAN ANCHOR BIOSYNTHESIS B in human, is required for Arabidopsis pollen tube micropylar guidance and embryo development. Plant Physiol 165:1544–1556
Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138:778–789
Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu HM, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129
Erdmann RM, Hoffmann A, Walter HK, Wagenknecht HA, Groß-Hardt R, Gehring M (2017) Molecular movement in the Arabidopsis thaliana female gametophyte. Plant Reprod 30:141–146
Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104:14531–14536
Gao QF, Gu LL, Wang HQ, Fei CF, Fang X, Hussain J, Sun SJ, Dong JY, Liu H, Wang YF (2016) Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc Natl Acad Sci USA 113:3096–3101
Ge Z, Bergonci T, Zhao Y, Zou Y, Du S, Liu MC, Luo X, Ruan H, García-Valencia LE, Zhong S, Hou S, Huang Q, Lai L, Moura DS, Gu H, Dong J, Wu HM, Dresselhaus T, Xiao J, Cheung AY, Qu LJ (2017) Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358:1596–1600
Guan Y, Lu J, Xu J, Mcclure B, Zhang S (2014) Two mitogen-activated protein kinases, MPK3 and MPK6, are required for funicular guidance of pollen tubes in Arabidopsis. Plant Physiol 165:528–533
Gui CP, Dong X, Liu HK, Huang WJ, Zhang D, Wang SJ, Barberini ML, Gao XY, Muschietti J, McCormick S, Tang WH (2014) Overexpression of the tomato pollen receptor kinase LePRK1 rewires pollen tube growth to a blebbing mode. Plant Cell 26:3538–3555
Hamamura Y, Nishimaki M, Takeuchi H, Geitmann A, Kurihara D, Higashiyama T (2014) Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat Commun 5:4722
Han YZ, Huang BQ, Zee SY, Yuan M (2000) Symplastic communication between the central cell and the egg apparatus cells in the embryo sac of Torenia fournieri Lind. before and during fertilization. Planta 211:158–162
Higashiyama T (2010) Peptide signaling in pollen-pistil interactions. Plant Cell Physiol 51:177–189
Higashiyama T, Takeuchi H (2015) The mechanism and key molecules involved in pollen tube guidance. Annu Rev Plant Biol 66:393–413
Higashiyama T, Yang WC (2017) Gametophytic pollen tube guidance: attractant peptides, gametic controls, and receptors. Plant Physiol 173:112–121
Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (1998) Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri. Plant Cell 10:2019–2032
Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 293:1480–1483
Huang WJ, Liu HK, McCormick S, Tang WH (2014) Tomato pistil factor STIG1 promotes in vivo pollen tube growth by binding to phosphatidylinositol 3-phosphate and the extracellular domain of the pollen receptor kinase LePRK2. Plant Cell 26:2505–2523
Huang Q, Dresselhaus T, Gu H, Qu LJ (2015) Active role of small peptides in Arabidopsis reproduction: expression evidence. J Integr Plant Biol 57:518–521
Ischebeck T (2016) Lipids in pollen—they are different. Biochim Biophys Acta 1861:1315–1328
Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, Sundaresan V, Ye D (2005) VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–596
Kagi C, Baumann N, Nielsen N, Stierhof YD, Gross-Hardt R (2010) The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells. Proc Natl Acad Sci USA 107:22350–22355
Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazaki T, Senzaki E, Hamamura Y, Higashiyama T, Takayama S, Abe M, Kuchitsu K (2014) Ca2+-activated reactive oxygen species production by Arabidopsis RbohH and RbohJ is essential for proper pollen tube tip growth. Plant Cell 26:1069–1080
Kim HU, Cotter R, Johnson S, Senda M, Dodds P, Kulikauska R, Tang W, Ezcura I, Herzmark P, McCormick S (2002) New pollen-specific receptor kinases identified in tomato, maize and Arabidopsis: the tomato kinases show overlapping but distinct localization patterns on pollen tubes. Plant Mol Biol 50:1–16
Kim S, Mollet JC, Dong J, Zhang K, Park SY, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100:16125–16130
Kim HJ, Ok SH, Bahn SC, Jang J, Oh SA, Park SK, Twell D, Ryu SB, Shin JS (2011) Endoplasmic reticulum- and Golgi-localized phospholipase A2 plays critical roles in Arabidopsis pollen development and germination. Plant Cell 23:94–110
Kobayashi M, Ohura I, Kawakita K, Yokota N, Fujiwara M, Shimamoto K, Doke N, Yoshioka H (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19:1065–1080
Krohn NG, Lausser A, Juranic M, Dresselhaus T (2012) Egg cell signaling by the secreted peptide ZmEAL1 controls antipodal cell fate. Dev Cell 23:219–225
Lassig R, Gutermuth T, Bey TD, Konrad KR, Romeis T (2014) Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. Plant J 78:94–106
Leydon AR, Weinreb C, Venable E, Reinders A, Ward JM, Johnson MA (2017) The molecular dialog between flowering plant reproductive partners defined by SNP-informed RNA-sequencing. Plant Cell 29:984–1006
Li HJ, Yang WC (2012) Emerging role of ER quality control in plant cell signal perception. Protein Cell 3:10–16
Li HJ, Yang WC (2016) RLKs orchestrate the signaling in plant male-female interaction. Sci China Life Sci 59:867–877
Li HJ, Xue Y, Jia DJ, Wang T, Hi DQ, Liu J, Cui F, Xie Q, Ye D, Yang WC (2011) POD1 regulates pollen tube guidance in response to micropylar female signaling and acts in early embryo patterning in Arabidopsis. Plant Cell 23:3288–3302
Li S, Ge FR, Xu M, Zhao XY, Huang GQ, Zhou LZ, Wang JG, Kombrink A, McCormick S, Zhang XS, Zhang Y (2013) Arabidopsis COBRA-LIKE 10, a GPI-anchored protein, mediates directional growth of pollen tubes. Plant J 74:486–497
Li HJ, Zhu SS, Zhang MX, Wang T, Liang L, Xue Y, Shi DQ, Liu JA, Yang WC (2015) Arabidopsis CBP1 is a novel regulator of transcription initiation in central cell-mediated pollen tube guidance. Plant Cell 27:2880–2893
Lin SY, Chen PW, Chuang MH, Juntawong P, Bailey-Serres J, Jauh GY (2014) Profiling of translatomes of in vivo-grown pollen tubes reveals genes with roles in micropylar guidance during pollination in Arabidopsis. Plant Cell 26:602–618
Liu J, Zhong S, Guo X, Hao L, Wei X, Hou Y, Shi J, Huang Q, Wang C, Gu H, Qu LJ (2013) Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr Biol 23:1–6
Liu L, Zheng C, Kuang B, Wei L, Yan L, Wang T (2016) Receptor-like kinase RUPO interacts with potassium transporters to regulate pollen tube growth and integrity in rice. PLoS Genet 12:e1006085
Loraine AE, Mccormick S, Estrada A, Patel K, Qin P (2013) RNA-seq of Arabidopsis pollen uncovers novel transcription and alternative splicing. Plant Physiol 162:1092–1109
Lord E (2000) Adhesion and cell movement during pollination: cherchez la femme. Trends Plant Sci 5:368–373
Lu Y, Chanroj S, Zulkifli L, Johnson MA, Uozumi N, Cheung A, Sze H (2011) Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis. Plant Cell 23:81–93
Mangano S, Juarez SP, Estevez JM (2016) ROS regulation of polar growth in plant cells. Plant Physiol 171:1593–1605
Márton ML, Cordts S, Broadhvest J, Dresselhaus T (2005) Micropylar pollen tube guidance by egg apparatus 1 of maize. Science 307:573–576
Maruyama D, Endo T, Nishikawa S (2010) BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. Proc Natl Acad Sci USA 107:1684–1689
Maruyama D, Sugiyama T, Endo T, Nishikawa S (2014) Multiple BiP genes of Arabidopsis thaliana are required for male gametogenesis and pollen competitiveness. Plant Cell Physiol 55:801–810
Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, Gagliardini V, Martínez-Bernardini A, Fabrice TN, Ringli C, Muschietti JP, Grossniklaus U (2017) RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358:1600–1603
Michard E, Simon AA, Tavares B, Wudick MM, Feijo JA (2017) Signaling with Ions: the keystone for apical cell growth and morphogenesis in pollen tubes. Plant Physiol 173:91–111
Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, Fukuda H, Hasebe M (2009) ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr Biol 19:1327–1331
Mizukami AG, Inatsugi R, Jiao J, Kotake T, Kuwata K, Ootani K, Okuda S, Sankaranarayanan S, Sato Y, Maruyama D, Iwai H, Garénaux E, Sato C, Kitajima K, Tsumuraya Y, Mori H, Yamaguchi J, Itami K, Sasaki N, Higashiyama T (2016) The AMOR arabinogalactan sugar chain induces pollen-tube competency to respond to ovular guidance. Curr Biol 26:1091–1097
Morato do Canto A, Ceciliato PH, Ribeiro B, Ortiz Morea FA, Franco Garcia AA, Silva-Filho MC, Moura DS (2014) Biological activity of nine recombinant AtRALF peptides: implications for their perception and function in Arabidopsis. Plant Physiol Biochem 75:45–54
Mouline K, Véry 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 16:339–350
Mu JH, Lee HS, Kao TH (1994) Characterization of a pollen-expressed receptor-like kinase gene of Petunia inflata and the activity of its encoded kinase. Plant Cell 6:709–721
Murphy E, De Smet I (2014) Understanding the RALF family: a tale of many species. Trends Plant Sci 19:664–671
Muschietti J, Eyal Y, McCormick S (1998) Pollen tube localization implies a role in pollen-pistil interactions for the tomato receptor-like protein kinases LePRK1 and LePRK2. Plant Cell 10:319–330
Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U (2014) A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev Cell 29:491–500
Nissen KS, Willats WG, Malinovsky FG (2016) Understanding CrRLK1L function: cell walls and growth control. Trend Plant Sci 21:516–5271
Okuda S, Tsutsui H, Shiina K, Sprunck S, Takeuchi H, Yui R, Kasahara RD, Hamamura Y, Mizukami A, Susaki D, Kawano N, Sakakibara T, Namiki S, Itoh K, Otsuka K, Matsuzaki M, Nozaki H, Kuroiwa T, Nakano A, Kanaoka MM, Dresselhaus T, Sasaki N, Higashiyama T (2009) Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458:357–361
Palanivelu R, Brass L, Edlund AF, Preuss D (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59
Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18:1862–1872
Potocký M, Pejchar P, Gutkowska M, Jiménez-Quesada MJ, Potocká A, Alché Jde D, Kost B, Žárský V (2012) NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J Plant Physiol 169:1654–1663
Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542
Schiott M, Romanowsky SM, Baekgaard L, Jakobsen MK, Palmgren MG, Harper JF (2004) A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101:9502–9507
Shimizu KK, Ito T, Ishiguro S, Okada K (2008) MAA3 (MAGATAMA3) helicase gene is required for female gametophyte development and pollen tube guidance in Arabidopsis thaliana. Plant Cell Physiol 49:1478
Steffen JG, Kang IH, Portereiko MF, Lloyd A, Drews GN (2008) AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol 148:259–268
Steinhorst L, Mähs A, Ischebeck T, Zhang C, Zhang X, Arendt S, Schültke S, Heilmann I, Kudla J (2015) Vacuolar CBL-CIPK12 Ca2+-sensor-kinase complexes are required for polarized pollen tube growth. Curr Biol 25:1475–1482
Susaki D, Takeuchi H, Tsutsui H, Kurihara D, Higashiyama T (2015) Live imaging and laser disruption reveal the dynamics and cell-cell communication during Torenia fournieri female gametophyte development. Plant Cell Physiol 56:1031–1041
Takeuchi H, Higashiyama T (2011) Attraction of tip-growing pollen tubes by the female gametophyte. Curr Opin Plant Biol 14:614–621
Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10:e1001449
Takeuchi H, Higashiyama T (2016) Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245–248
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
Tang W, Kelley D, Ezcurra I, Cotter R, McCormick S (2004) LeSTIG1, an extracellular binding partner for the pollen receptor kinases LePRK1 and LePRK2, promotes pollen tube growth in vitro. Plant J 39:343–353
Uebler S, Dresselhaus T, Márton ML (2014) Species-specific interaction of EA1 with the maize pollen tube apex. Plant Signal Behav 8:e25682
Vogler H, Draeger C, Weber A, Felekis D, Eichenberger C, Routier-Kierzkowska AL, Boisson-Dernier A, Ringli C, Nelson BJ, Smith RS, Grossniklaus U (2012) The pollen tube: a soft shell with a hard core. Plant J 73:617–627
Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211
Wang L, Wang W, Wang YQ, Liu YY, Wang JX, Zhang XQ, Ye D, Chen LQ (2013) Arabidopsis galacturonosyltransferase (GAUT) 13 and GAUT14 have redundant functions in pollen tube growth. Mol Plant 6:1131–1148
Wang SS, Diao WZ, Yang X, Qiao Z, Wang M, Acharya BR, Zhang W (2015) Arabidopsis thaliana CML25 mediates the Ca2+ regulation of K+ transmembrane trafficking during pollen germination and tube elongation. Plant Cell Environ 38:2372–2386
Wang T, Liang L, Xue Y, Jia PF, Chen W, Zhang MX, Wang YC, Li HJ, Yang WC (2016a) A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:241–244
Wang JG, Feng C, Liu HH, Ge FR, Li S, Li HJ, Zhang Y (2016b) HAPLESS13-mediated trafficking of STRUBBELIG is critical for ovule development in Arabidopsis. PLoS Genet 12:e1006269
Wang JG, Feng C, Liu HH, Feng QN, Li S, Zhang Y (2017) AP1G mediates vacuolar acidification during synergid-controlled pollen tube reception. Proc Natl Acad Sci USA 114:E4877–E4883
Winship LJ, Obermeyer G, Geitmann A, Hepler PK (2011) Pollen tubes and the physical world. Trends Plant Sci 16:353–355
Woriedh M, Wolf S, Márton ML, Hinze A, Gahrtz M, Becker D, Dresselhaus T (2013) External application of gametophyte-specific ZmPMEI1 induces pollen tube burst in maize. Plant Reprod 26:255–266
Wu J, Qin X, Tao S, Jiang X, Liang YK, Zhang S (2014) Long-chain base phosphates modulate pollen tube growth via channel-mediated influx of calcium. Plant J 79:507–516
Xu Y, Yang J, Wang Y, Wang J, Yu Y, Long Y, Wang Y, Zhang H, Ren Y, Chen J, Wang Y, Zhang X, Guo X, Wu F, Zhu S, Lin Q, Jiang L, Wu C, Wang H, Wan J (2017) OsCNGC13 promotes seed-setting rate by facilitating pollen tube growth in stylar tissues. PLoS Genet 13:e1006906
Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61:89–108
Yang X, Wang SS, Wang M, Qiao Z, Bao CC, Zhang W (2014) Arabidopsis thaliana calmodulin-like protein CML24 regulates pollen tube growth by modulating the actin cytoskeleton and controlling the cytosolic Ca2+ concentration. Plant Mol Biol 86:225–236
Zhang Y, McCormick S (2007) A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. Proc Natl Acad Sci USA 104:18830–18835
Zhang X, Liu W, Nagae TT, Takeuchi H, Zhang H, Han Z, Higashiyama T, Chai J (2017) Structural basis for receptor recognition of pollen tube attraction peptides. Nat Commun 8:1331
Zhao LN, Shen LK, Zhang WZ, Zhang W, Wang Y, Wu WH (2013) Ca2+-dependent protein kinase 11 and 24 modulate the activity of the inward rectifying K+ channels in Arabidopsis pollen tubes. Plant Cell 25:649–661
Zhou L, Lan W, Chen B, Fang W, Luan S (2015) A calcium sensor-regulated protein kinase, CALCINEURIN B-LIKE PROTEIN-INTERACTING PROTEIN KINASE19, is required for pollen tube growth and polarity. Plant Physiol 167:1351–1360
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This work is supported by the Grant from National Natural Science Foundation of China (31571385, 31622010 to H. L. and 31330053 to W. Y.).
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Communicated by Tetsuya Higashiyama.
A contribution to the special issue ‘Plant Reproduction Research in Asia’.
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Li, HJ., Meng, JG. & Yang, WC. Multilayered signaling pathways for pollen tube growth and guidance. Plant Reprod 31, 31–41 (2018). https://doi.org/10.1007/s00497-018-0324-7
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DOI: https://doi.org/10.1007/s00497-018-0324-7