Advance Search
Liu XF，Sun MX，Peng XB. Molecular basis of pollen tube guidance and avoidance of polytubey fertilization[J]. Plant Science Journal，2023，41（1）：128−137. DOI: 10.11913/PSJ.2095-0837.22082
Citation: Liu XF，Sun MX，Peng XB. Molecular basis of pollen tube guidance and avoidance of polytubey fertilization[J]. Plant Science Journal，2023，41（1）：128−137. DOI: 10.11913/PSJ.2095-0837.22082
shu

Molecular basis of pollen tube guidance and avoidance of polytubey fertilization

  • State Key Laboratory of Hybrid Rice, College of Life Sciences, Wuhan University, Wuhan 430072, China

Funds: This work was supported by a grant from the National Natural Science Foundation of China (31870302)
More Information
  • Received Date: June 30, 2022
  • Revised Date: August 29, 2022
  • Available Online: March 02, 2023
    Graphical Abstract
    • Abstract

  • In angiosperms, mature pollen falls on the stigma to germinate the pollen tube. Under the guidance of funiculus and micropyle signals, the pollen tube grows accurately into the embryo sac in the ovule, and then ruptures to release two sperm cells to complete double fertilization. Ensuring that only one pollen tube enters the embryo sac for complete double fertilization and stable transmission of genetic information is carefully regulated. This paper reviews recent research on the mechanisms of pollen tube guidance and polytubey block.

    • FullText(HTML)
    • References (59)
  • [1]
    Wei DH,Liu MJ,Chen H,Zheng Y,Liu YX,et al. INDUCER OF CBF EXPRESSION 1 is a male fertility regulator impacting anther dehydration in Arabidopsis[J]. PLoS Genet,2018,14 (10):e1007695. doi: 10.1371/journal.pgen.1007695
    [2]
    Shi DQ, Yang WC. Pollen germination and tube growth [M] // Pua EC, Davey MR, eds. Plant Developmental Biology-Biotechnological Perspectives: Vol 1. Berlin, Heidelberg: Springer, 2010: 245-282.
    [3]
    Edlund AF,Swanson R,Preuss D. Pollen and stigma structure and function:the role of diversity in pollination[J]. Plant Cell,2004,16 (S1):S84−S97.
    [4]
    Jiang LX,Yang SL,Xie LF,Puah CS,Zhang XQ,et al. VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the arabidopsis style and transmitting tract[J]. Plant Cell,2005,17 (2):584−596. doi: 10.1105/tpc.104.027631
    [5]
    Higashiyama T,Kuroiwa H,Kuroiwa T. Pollen-tube guidance:beacons from the female gametophyte[J]. Curr Opin Plant Biol,2003,6 (1):36−41. doi: 10.1016/S1369-5266(02)00010-9
    [6]
    Faure JE. Double fertilization in flowering plants:discovery,study methods and mechanisms[J]. C R Acad Sci Ⅲ,2001,324 (6):551−558. doi: 10.1016/S0764-4469(01)01325-7
    [7]
    Dresselhaus T. Cell-cell communication during double fertilization[J]. Curr Opin Plant Biol,2006,9 (1):41−47. doi: 10.1016/j.pbi.2005.11.002
    [8]
    Kim MJ,Jeon BW,Oh E,Seo PJ,Kim J. Peptide signaling during plant reproduction[J]. Trends Plant Sci,2021,26 (8):822−835. doi: 10.1016/j.tplants.2021.02.008
    [9]
    Zhang JH,Yue L,Wu XL,Liu H,Wang W. Function of small peptides during male-female crosstalk in plants[J]. Front Plant Sci,2021,12:671196. doi: 10.3389/fpls.2021.671196
    [10]
    Ray SM,Park SS,Ray A. Pollen tube guidance by the female gametophyte[J]. Development,1997,124 (12):2489−2498. doi: 10.1242/dev.124.12.2489
    [11]
    Schiefthaler U,Balasubramanian S,Sieber P,Chevalier D,Wisman E,Schneitz K. Molecular analysis of NOZZLE,a gene involved in pattern formation and early sporogenesis during sex organ development in Arabidopsis thaliana[J]. Proc Natl Acad Sci USA,1999,96 (20):11664−11669. doi: 10.1073/pnas.96.20.11664
    [12]
    Yang WC,Ye D,Xu J,Sundaresan V. The SPOROCYTELESS gene of Arabidopsis is required for initiation of sporogenesis and encodes a novel nuclear protein[J]. Genes Dev,1999,13 (16):2108−2117. doi: 10.1101/gad.13.16.2108
    [13]
    Wang HZ,Boavida LC,Ron M,McCormick S. Truncation of a protein disulfide isomerase,PDIL2-1,delays embryo sac maturation and disrupts pollen tube guidance in Arabidopsis thaliana[J]. Plant Cell,2008,20 (12):3300−3311.
    [14]
    Kulichová K,Kumar V,Steinbachová L,Klodová B,Timofejeva L,et al. PRP8A and PRP8B spliceosome subunits act coordinately to control pollen tube attraction in Arabidopsis thaliana[J]. Development,2020,147 (11):dev186742.
    [15]
    Guan YF,Lu JP,Xu J,Mcclure B,Zhang SQ. Two mitogen-activated protein kinases,MPK3 and MPK6,are required for funicular guidance of pollen tubes in Arabidopsis[J]. Plant Physiol,2014,165 (2):528−533. doi: 10.1104/pp.113.231274
    [16]
    Lu YX,Chanroj S,Zulkifli L,Johnson MA,Uozumi N,et al. Pollen tubes lacking a pair of K+ transporters fail to target ovules in Arabidopsis[J]. Plant Cell,2011,23 (1):81−93. doi: 10.1105/tpc.110.080499
    [17]
    Jensen WA,Fisher DB. Cotton embryogenesis:the entrance and discharge of the pollen tube in the embryo sac[J]. Planta,1967,78 (2):158−183. doi: 10.1007/BF00406648
    [18]
    Tian HQ,Russell SD. Calcium distribution in fertilized and unfertilized ovules and embryo sacs of Nicotiana tabacum L.[J]. Planta,1997,202 (1):93−105. doi: 10.1007/s004250050107
    [19]
    Iwano M,Ngo QA,Entani T,Shiba H,Nagai T,et al. Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells[J]. Development,2012,139 (22):4202−4209. doi: 10.1242/dev.081208
    [20]
    Tian HQ,Zhu H,Russell SD. Calcium changes in ovules and embryo sacs of Plumbago zeylanica L.[J]. Sex Plant Reprod,2000,13 (1):11−20. doi: 10.1007/PL00009837
    [21]
    Hamamura Y,Nishimaki M,Takeuchi H,Geitmann A,Kurihara D,Higashiyama T. Live imaging of calcium spikes during double fertilization in Arabidopsis[J]. Nat Commun,2014,5:4722. doi: 10.1038/ncomms5722
    [22]
    Christensen CA,Gorsich SW,Brown RH,Jones LG,Brown J,et al. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis[J]. Plant Cell,2002,14 (9):2215−2232. doi: 10.1105/tpc.002170
    [23]
    Maruyama D,Völz R,Takeuchi H,Mori T,Igawa T,et al. Rapid elimination of the persistent synergid through a cell fusion mechanism[J]. Cell,2015,161 (4):907−918. doi: 10.1016/j.cell.2015.03.018
    [24]
    Rotman N,Rozier F,Boavida L,Dumas C,Berger F,Faure JE. Female control of male gamete delivery during fertilization in Arabidopsis thaliana[J]. Curr Biol,2003,13 (5):432−436. doi: 10.1016/S0960-9822(03)00093-9
    [25]
    Kasahara RD,Portereiko MF,Sandaklie-Nikolova L,Rabiger DS,Drews GN. MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis[J]. Plant Cell,2005,17 (11):2981−2992. doi: 10.1105/tpc.105.034603
    [26]
    Erdelská O,Vidovencová Z,Erdelský K. Cleavage polyembryos as explants for plant regeneration in wheat[J]. Plant Cell Rep,1996,15 (5):342−344. doi: 10.1007/BF00232368
    [27]
    Higashiyama T,Kuroiwa H,Kawano S,Kuroiwa T. Guidance in vitro of the pollen tube to the naked embryo sac of Torenia fournieri[J]. Plant Cell,1998,10 (12):2019−2031. doi: 10.1105/tpc.10.12.2019
    [28]
    Higashiyama T,Inatsugi R,Sakamoto S,Sasaki N,Mori T,et al. Species preferentiality of the pollen tube attractant derived from the synergid cell of Torenia fournieri[J]. Plant Physiol,2006,142 (2):481−491. doi: 10.1104/pp.106.083832
    [29]
    Higashiyama T,Kuroiwa H,Kawano S,Kuroiwa T. Explosive discharge of pollen tube contents in Torenia fournieri[J]. Plant Physiol,2000,122 (1):11−14. doi: 10.1104/pp.122.1.11
    [30]
    Higashiyama T,Yabe S,Sasaki N,Nishimura Y,Miyagishima SY,et al. Pollen tube attraction by the synergid cell[J]. Science,2001,293 (5534):1480−1483. doi: 10.1126/science.1062429
    [31]
    Okuda S,Tsutsui H,Shiina K,Sprunck S,Takeuchi H,et al. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells[J]. Nature,2009,458 (7236):357−361. doi: 10.1038/nature07882
    [32]
    Takeuchi H,Higashiyama T. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis[J]. PLoS Biol,2012,10 (12):e1001449. doi: 10.1371/journal.pbio.1001449
    [33]
    Zhong S,Liu ML,Wang ZJ,Huang QP,Hou SY,et al. Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis[J]. Science,2019,364 (6443):eaau9564. doi: 10.1126/science.aau9564
    [34]
    Mizukami AG,Inatsugi R,Jiao J,Kotake T,Kuwata K,et al. The AMOR arabinogalactan sugar chain induces pollen-tube competency to respond to ovular guidance[J]. Curr Biol,2016,26 (8):1091−1097. doi: 10.1016/j.cub.2016.02.040
    [35]
    Takeuchi H,Higashiyama T. Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis[J]. Nature,2016,531 (7593):245−248. doi: 10.1038/nature17413
    [36]
    Wang T,Liang L,Xue Y,Jia PF,Chen W,et al. A receptor heteromer mediates the male perception of female attractants in plants[J]. Nature,2016,531 (7593):241−244. doi: 10.1038/nature16975
    [37]
    Liu JJ,Zhong S,Guo XY,Hao LH,Wei XL,et al. Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis[J]. Curr Biol,2013,23 (11):993−998. doi: 10.1016/j.cub.2013.04.043
    [38]
    Gao QF,Gu LL,Wang HQ,Fei CF,Fang X,et al. Cyclic nucleotide-gated channel 18 is an essential Ca2 + channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis[J]. Proc Natl Acad Sci USA,2016,113 (11):3096−3101. doi: 10.1073/pnas.1524629113
    [39]
    Meng JG,Liang L,Jia PF,Wang YC,Li HJ,Yang WC. Integration of ovular signals and exocytosis of a Ca2 + channel by MLOs in pollen tube guidance[J]. Nat Plants,2020,6 (2):143−153. doi: 10.1038/s41477-020-0599-1
    [40]
    Márton ML,Cordts S,Broadhvest J,Dresselhaus T. Micropylar pollen tube guidance by egg apparatus 1 of maize[J]. Science,2005,307 (5709):573−576. doi: 10.1126/science.1104954
    [41]
    Márton ML,Fastner A,Uebler S,Dresselhaus T. Overcoming hybridization barriers by the secretion of the maize pollen tube attractant ZmEA1 from Arabidopsis ovules[J]. Curr Biol,2012,22 (13):1194−1198. doi: 10.1016/j.cub.2012.04.061
    [42]
    Chen YH,Li HJ,Shi DQ,Yuan L,Liu J,et al. The central cell plays a critical role in pollen tube guidance in Arabidopsis[J]. Plant Cell,2007,19 (11):3563−3577. doi: 10.1105/tpc.107.053967
    [43]
    Li HJ,Zhu SS,Zhang MX,Wang T,Liang L,et al. Arabidopsis CBP1 is a novel regulator of transcription initiation in central cell-mediated pollen tube guidance[J]. Plant Cell,2015,27 (10):2880−2893. doi: 10.1105/tpc.15.00370
    [44]
    Huck N,Moore JM,Federer M,Grossniklaus U. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception[J]. Development,2003,130 (10):2149−2159. doi: 10.1242/dev.00458
    [45]
    Escobar-Restrepo JM,Huck N,Kessler S,Gagliardini V,Gheyselinck J,et al. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception[J]. Science,2007,317 (5838):656−660. doi: 10.1126/science.1143562
    [46]
    Kessler SA,Lindner H,Jones DS,Grossniklaus U. Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception[J]. EMBO Rep,2015,16 (1):107−115. doi: 10.15252/embr.201438801
    [47]
    Zhong S,Li L,Wang ZJ,Ge ZX,Li QY,et al. RALF peptide signaling controls the polytubey block in Arabidopsis[J]. Science,2022,375 (6578):290−296. doi: 10.1126/science.abl4683
    [48]
    Duan QH,Liu MCJ,Kita D,Jordan SS,Yeh FLJ,et al. FERONIA controls pectin- and nitric oxide-mediated male-female interaction[J]. Nature,2020,579 (7800):561−566. doi: 10.1038/s41586-020-2106-2
    [49]
    Kasahara RD,Maruyama D,Hamamura Y,Sakakibara T,Twell D,et al. Fertilization recovery after defective sperm cell release in Arabidopsis[J]. Curr Biol,2012,22 (12):1084−1089. doi: 10.1016/j.cub.2012.03.069
    [50]
    Beale KM,Leydon AR,Johnson MA. Gamete fusion is required to block multiple pollen tubes from entering an Arabidopsis ovule[J]. Curr Biol,2012,22 (12):1090−1094. doi: 10.1016/j.cub.2012.04.041
    [51]
    Mori T,Kuroiwa H,Higashiyama T,Kuroiwa T. GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization[J]. Nat Cell Biol,2006,8 (1):64−71. doi: 10.1038/ncb1345
    [52]
    Maruyama D,Hamamura Y,Takeuchi H,Susaki D,Nishimaki M,et al. Independent control by each female gamete prevents the attraction of multiple pollen tubes[J]. Dev Cell,2013,25 (3):317−323. doi: 10.1016/j.devcel.2013.03.013
    [53]
    Aw SJ,Hamamura Y,Chen Z,Schnittger A,Berger F. Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis[J]. Development,2010,137 (16):2683−2690. doi: 10.1242/dev.052928
    [54]
    Köhler C,Wolff P,Spillane C. Epigenetic mechanisms underlying genomic imprinting in plants[J]. Annu Rev Plant Biol,2012,63:331−352. doi: 10.1146/annurev-arplant-042811-105514
    [55]
    Hennig L,Derkacheva M. Diversity of polycomb group complexes in plants:same rules,different players?[J]. Trends Genet,2009,25 (9):414−423. doi: 10.1016/j.tig.2009.07.002
    [56]
    Chaudhury AM,Ming L,Miller C,Craig S,Dennis ES,Peacock WJ. Fertilization-independent seed development in Arabidopsis thaliana[J]. Proc Natl Acad Sci USA,1997,94 (8):4223−4228. doi: 10.1073/pnas.94.8.4223
    [57]
    Ohad N,Yadegari R,Margossian L,Hannon M,Michaeli D,et al. Mutations in FIE,a WD polycomb group gene,allow endosperm development without fertilization[J]. Plant Cell,1999,11 (3):407−415. doi: 10.1105/tpc.11.3.407
    [58]
    Yu XB,Zhang XC,Zhao P,Peng XB,Chen H,et al. Fertilized egg cells secrete endopeptidases to avoid polytubey[J]. Nature,2021,592 (7854):433−437. doi: 10.1038/s41586-021-03387-5
    [59]
    Dai XR,Gao XQ,Chen GH,Tang LL,Wang H,Zhang XS. 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[J]. Plant Physiol,2014,165 (4):1544−1556. doi: 10.1104/pp.114.236133
    • Related Articles

  • Related Articles

    [1]Niu Xue-Jing, Nie Jing, Zhao Xue-Li, Gao Xin-Fen. Leaf-level phenotypic plasticity of Indigofera bungeana Walp.[J]. Plant Science Journal, 2020, 38(1): 97-104. DOI: 10.11913/PSJ.2095-0837.2020.10097
    [2]FAN Xiang-Rong, LI Zhi, CHU Hai-Jia, LI Wei, LIU Yan-Ling, CHEN Yuan-Yuan. Analysis of Morphological Plasticity of Trapa L. from China and Their Taxonomic Significance[J]. Plant Science Journal, 2016, 34(3): 340-351. DOI: 10.11913/PSJ.2095-0837.2016.30340
    [3]DAI Can, QIN Dao-Feng, LUO Wen-Jie. Ecological and Evolutionary Studies on Sagittaria (Alismataceae)[J]. Plant Science Journal, 2015, 33(5): 620-632. DOI: 10.11913/PSJ.2095-0837.2015.50620
    [4]GAO Le-Xuan. Comparisons of Morphological Variation and Cellular Osmotic Potential Adjustment between Invasive Species Alternanthera philoxeroides and its Native Congener A. sessilis under Different Water Treatments[J]. Plant Science Journal, 2015, 33(2): 195-202. DOI: 10.11913/PSJ.2095-0837.2015.20195
    [5]DENG Ying, GAO Le-Xuan, ZHU Zhu, YANG Ji. Differential Expression of DNA Methylation Regulating Factors and Dynamic Methylation Patterns of Alternanthera philoxeroides under Different Water Treatments[J]. Plant Science Journal, 2014, 32(5): 475-486. DOI: 10.11913/PSJ.2095-0837.2014.50475
    [6]LIAO Ling-Juan, LI-Qing, CHEN Yi-Zhu, LIN Jun-Xin, WU Lin-Fang, CAO Hong-Lin. Effects of Environmental Disturbance on Leaf Morphological Traits, Stomata, and Water Use Efficiency of Species for Afforestation on a Windward Slope in a Coastal Zone[J]. Plant Science Journal, 2011, 1(5): 613-624.
    [7]HU Ying, CHU Hai-Jia, LI Jian-Qiang. Response of Leaf Anatomy Characteristics and Its Plasticity to Different Soil-water Conditions of Medicago ruthenica in Four Populations[J]. Plant Science Journal, 2011, 29(2): 218-225.
    [8]SUN Xiao-Fang, REN Ming-Xun, WANG Gang, TAN Gen-Jia, HE Jia-Qing, HUANG Xun-Duan, PING Jiang, GE Jie-Lin. Photosynthetic Physiology and Clonal Growth of Solidago canadensis at Different Light Intensities:Implications for Invasive Mechanism[J]. Plant Science Journal, 2008, 26(6): 620-626.
    [9]LI Qing-Yu, ZHONG Zhang-Cheng, HE Yue-Jun. Effects of Soil Nutrients on Plasticity of Floral Characteristics in Iris japonica Thunb.[J]. Plant Science Journal, 2005, 23(6): 564-567.
    [10]XU Kai-Yang, YE Wan-Hui, LI Guo-Min, LI Jing. Phenotypic Plasticity in Response to Light Intensity in the Invasive Species Alternanthera philoxeroides[J]. Plant Science Journal, 2005, 23(6): 560-563.

  • Cited by

    Periodical cited type(6)

    1. 柏晓瑜，林韶娟，郑城浩，刘凯良，叶祖云，王振华. 高温热浪对亚热带园林植物危害的调查分析. 热带亚热带植物学报. 2025(01): 57-64 .
    2. 傅志强，张恒，刘祯，奚如春. 不同油茶品种苗对高温胁迫的生理响应及耐热性评价. 林业科学研究. 2024(02): 189-200 .
    3. 黄淦，李美婷，赵艳莉，曹琴，张新，李菲，李永华，王亚琴. 不同切花菊品种的高温生理响应及耐热性综合评价. 华南师范大学学报(自然科学版). 2024(01): 92-103 .
    4. 常翠芳，郭丽娟，于宏，韩亚梅，朱景乐，武荣花. 四个长阶花品种叶片对高温胁迫形态及生理响应. 北方园艺. 2024(11): 56-63 .
    5. 田维新. 高海拔冷凉区大丽花冬藏—春栽—秋收管理技术. 西北园艺. 2024(06): 31-34 .
    6. 刘屿洲，顾小煜，杨凤娟，李兴盛，袁晓伟，季托，李静. 耐高温胁迫西葫芦种质资源评价和筛选. 山东农业大学学报(自然科学版). 2024(05): 804-813 .

    Other cited types(2)

Catalog

    Get Citation
    PDF
    XML
    Article views (256) PDF downloads (51) Cited by(8)
    Turn off MathJax
    Article Contents
    Abstract
    References
    Related Articles
    Copyright © 2022 Plant Science Journal 鄂ICP备05004779号-3
    Address：No. 201, Jiufeng 1st Road, Donghu High tech Zone, WuhanPostal Code：430074

    Supported by: Beijing Renhe Information Technology Co., Ltd.  Baidu Analytics

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return