Abstract
Key message
In light of the available discoveries in the field, this review manuscript discusses on plant reproduction mechanism and molecular players involved in the process.
Abstract
Sperm cells in angiosperms are immotile and are physically distant to the female gametophytes (FG). To secure the production of the next generation, plants have devised a clever approach by which the two sperm cells in each pollen are safely delivered to the female gametophyte where two fertilization events occur (by each sperm cell fertilizing an egg cell and central cell) to give rise to embryo and endosperm. Each of the successfully fertilized ovules later develops into a seed. Sets of macromolecules play roles in pollen tube (PT) guidance, from the stigma, through the transmitting tract and funiculus to the micropylar end of the ovule. Other sets of genetic players are involved in PT reception and in its rupture after it enters the ovule, and yet other sets of genes function in gametic fusion. Angiosperms have come long way from primitive reproductive structure development to today’s sophisticated, diverse, and in most cases flamboyant organ. In this review, we will be discussing on the intricate yet complex molecular mechanism of double fertilization and how it might have been shaped by the evolutionary forces focusing particularly on the model plant Arabidopsis.
Similar content being viewed by others
Abbreviations
- FG:
-
Female gametophyte
- EC:
-
Egg cell
- SC:
-
Synergid cell
- CC:
-
Central cell
- AC:
-
Antipodal cell
- Ca2+ :
-
Calcium
- NO:
-
Nitric oxide
- CHX:
-
Cation/H+ exchanger
- GSI:
-
Gametophytic self-incompatibility
- MP:
-
Micropyle
- PT:
-
Pollen tube
- POEM:
-
PT dependent ovule enlargement morphology
- ROS:
-
Reactive oxygen species
- SSI:
-
Sporophytic self-incompatibility
- TTS:
-
Transmitting tissue-specific
References
Aarts MGM, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira A (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12(3): 615–623. https://doi.org/10.1046/j.1365-313X.1997.00615.x
Albertini E, Barcaccia G, Carman JG, Pupilli F (2019) Did apomixis evolve from sex or was it the other way around? J Exp Bot 70(11):2951–2964. https://doi.org/10.1093/jxb/erz109
Alfieri A, Doccula FG, Pederzoli R, Grenzi M, Bonza MC, Luoni L, Candeo A, Romano Armada N, Barbiroli A, Valentini G, Schneider TR, Bassi A, Bolognesi M, Nardini M, Costa A (2020) The structural bases for agonist diversity in an Arabidopsis thaliana glutamate receptor-like channel. Proc Natl Acad Sci USA 117(1):752–760. https://doi.org/10.1073/pnas.1905142117
Alves CML, Noyszewski AK, Smith AG (2019) Nicotiana tabacum pollen–pistil interactions show unexpected spatial and temporal differences in pollen tube growth among genotypes. Plant Reproduction. https://doi.org/10.1007/s00497-019-00375-8
Amien S, Kliwer I, Márton ML, Debener T, Geiger D, Becker D, Dresselhaus T (2010) Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLoS Biol 8(6):e1000388. https://doi.org/10.1371/journal.pbio.1000388
Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyama K (2003) A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine. Plant Mol Biol 53(1):107–116. https://doi.org/10.1023/b:Plan.0000009269.97773.70
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875):977. https://doi.org/10.1038/415977a
Bai S-N (2015) The concept of the sexual reproduction cycle and its evolutionary significance. Front Plant Sci 6(11):11. https://doi.org/10.3389/fpls.2015.00011
Battat M, Eitan A, Rogachev I, Hanhineva K, Fernie A, Tohge T, Beekwilder J, Aharoni A (2019) A MYB triad controls primary and phenylpropanoid metabolites for pollen coat patterning. Plant Physiol 180(1):87–108. https://doi.org/10.1104/pp.19.00009
Baum DA, Whitlock BA (1999) Plant development: Genetic clues to petal evolution. Curr Biol 9(14):R525–R527. https://doi.org/10.1016/S0960-9822(99)80327-3
Beale KM, Leydon AR, Johnson MA (2012) Gamete fusion is required to block multiple pollen tubes from entering an Arabidopsis ovule. Curr Biol 22(12):1090–1094. https://doi.org/10.1016/j.cub.2012.04.041
Becks L, Agrawal AF (2012) The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10(5):e1001317. https://doi.org/10.1371/journal.pbio.1001317
Beeckman T, De Rycke R, Viane R, Inzé D (2000) Histological study of seed coat development in Arabidopsis thaliana. J Plant Res 113(2):139–148. https://doi.org/10.1007/pl00013924
Benko P, Jee S, Kaszler N, Feher A, Gemes K (2020) Polyamines treatment during pollen germination and pollen tube elongation in tobacco modulate reactive oxygen species and nitric oxide homeostasis. J Plant Physiol 244:153085. https://doi.org/10.1016/j.jplph.2019.153085
Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, Schroeder JI, Grossniklaus U (2009) Disruption of the pollen-expressed FERONIA homologs ANXUR11 and ANXUR2 triggers pollen tube discharge. Development 136(19):3279–3288. https://doi.org/10.1242/dev.040071
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(11):e1001719. https://doi.org/10.1371/journal.pbio.1001719
Bonza MC, Morandini P, Luoni L, Geisler M, Palmgren MG, De Michelis MI (2000) At-ACA8 encodes a plasma membrane-localized calcium-ATPase of Arabidopsis with a calmodulin-binding domain at the N terminus. Plant Physiol 123(4):1495–1506. https://doi.org/10.1104/pp.123.4.1495
Bower MS, Matias DD, Fernandes-Carvalho E, Mazzurco M, Gu T, Rothstein SJ, Goring DR (1996) Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 8(9):1641–1650. https://doi.org/10.1105/tpc.8.9.1641
Burri JT, Vogler H, Läubli NF, Hu C, Grossniklaus U, Nelson BJ (2018) Feeling the force: how pollen tubes deal with obstacles. New Phytol 220(1):187–195. https://doi.org/10.1111/nph.15260
Cabrillac D, Cock JM, Dumas C, Gaude T (2001) The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410(6825):220–223. https://doi.org/10.1038/35065626
Cao Y, Meng D, Chen T, Chen Y, Zeng W, Zhang L, Wang Q, Hen W, Abdullah M, Jin Q, Lin Y, Cai Y (2019) Metacaspase gene family in Rosaceae genomes: comparative genomic analysis and their expression during pear pollen tube and fruit development. PLoS ONE 14(2):e0211635. https://doi.org/10.1371/journal.pone.0211635
Capron A, Gourgues M, Neiva LS, Faure JE, Berger F, Pagnussat G, Krishnan A, Alvarez-Mejia C, Vielle-Calzada JP, Lee YR, Liu B, Sundaresan V (2008) Maternal control of male-gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. Plant Cell 20(11):3038–3049. https://doi.org/10.1105/tpc.108.061713
Chen D, Zhao J (2008) Free IAA in stigmas and styles during pollen germination and pollen tube growth of Nicotiana tabacum. Physiol Plant 134(1):202–215
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(11):3563–3577. https://doi.org/10.1105/tpc.107.053967
Cheung W (1980) Calmodulin plays a pivotal role in cellular regulation. Science 207(4426):19–27. https://doi.org/10.1126/science.6243188
Cheung AY, Wang H, Wu H-m (1995) A floral transmitting tissue-specific glycoprotein attracts pollen tubes and stimulates their growth. Cell 82(3):383–393
Christopher DA, Mitchell RJ, Karron JD (2020) Pollination intensity and paternity in flowering plants. Ann Bot 125(1):1–9. https://doi.org/10.1093/aob/mcz159
Clark G, Roux SJ (2011) Apyrases, extracellular ATP and the regulation of growth. Curr Opin Plant Biol 14(6):700–706. https://doi.org/10.1016/j.pbi.2011.07.013
Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353(6339):31–37. https://doi.org/10.1038/353031a0
Coimbra S, Costa M, Mendes MA, Pereira AM, Pinto J, Pereira LG (2010) Early germination of Arabidopsis pollen in a double null mutant for the arabinogalactan protein genes AGP6 and AGP11. Sex Plant Reprod 23(3):199–205. https://doi.org/10.1007/s00497-010-0136-x
Colombo L, Franken J, Koetje E, van Went J, Dons HJ, Angenent GC, van Tunen AJ (1995) The petunia MADS box gene FBP11 determines ovule identity. Plant Cell 7(11):1859–1868. https://doi.org/10.1105/tpc.7.11.1859
Colombo L, Franken J, Van der Krol AR, Wittich PE, Dons HJ, Angenent GC (1997) Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell 9(5):703–715. https://doi.org/10.1105/tpc.9.5.703
Costa M, Nobre MS, Becker JD, Masiero S, Amorim MI, Pereira LG, Coimbra S (2013) Expression-based and co-localization detection of arabinogalactan protein 6 and arabinogalactan protein 11 interactors in Arabidopsis pollen and pollen tubes. BMC Plant Biol 13(1):7. https://doi.org/10.1186/1471-2229-13-7
De Craene LPR (2010) Floral diagrams: an aid to understanding flower morphology and evolution. Cambridge University Press, Cambridge
Crawford BCW, Yanofsky MF (2011) HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 138(14):2999–3009. https://doi.org/10.1242/dev.067793
Crawford BCW, Ditta G, Yanofsky MF (2007) The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr Biol 17(13):1101–1108. https://doi.org/10.1016/j.cub.2007.05.079
Cyprys P, Lindemeier M, Sprunck S (2019) Gamete fusion is facilitated by two sperm cell-expressed DUF679 membrane proteins. Nat Plants 5(3):253–257. https://doi.org/10.1038/s41477-019-0382-3
Dellaert L, Van Es J, Koornneef M (1979) Eceriferum mutants in Arabidopsis thaliana (L.) Heynh. II. Phenotypic and genetic analysis. Arab Inf Serv 16(1):1
Dobritsa AA, Lei Z, Nishikawa S-I, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW (2010) LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153(3):937–955. https://doi.org/10.1104/pp.110.157446
Dong J, Kim ST, Lord EM (2005) Plantacyanin plays a role in reproduction in Arabidopsis. Plant Physiol 138(2):778–789. https://doi.org/10.1104/pp.105.063388
Doughty J, Hedderson F, McCubbin A, Dickinson H (1993) Interaction between a coating-borne peptide of the Brassica pollen grain and stigmatic S (self-incompatibility)-locus-specific glycoproteins. Proc Natl Acad Sci 90(2):467–471. https://doi.org/10.1073/pnas.90.2.467
Dresselhaus T, Márton ML (2009) Micropylar pollen tube guidance and burst: adapted from defense mechanisms? Curr Opin Plant Biol 12(6):773–780. https://doi.org/10.1016/j.pbi.2009.09.015
Dresselhaus T, Lörz H, Kranz E (1994) Representative cDNA libraries from few plant cells. Plant J 5(4):605–610. https://doi.org/10.1046/j.1365-313X.1994.05040605.x
Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu H-M, Cheung AY (2014) Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun 5:3129. https://doi.org/10.1038/ncomms4129
Endress PK (1986) Reproductive structures and phylogenetic significance of extant primitive angiosperms. Plant Syst Evol 152(1):1–28. https://doi.org/10.1007/bf00985348
Erdmann RM, Hoffmann A, Walter H-K, Wagenknecht H-A, Groß-Hardt R, Gehring M (2017) Molecular movement in the Arabidopsis thaliana female gametophyte. Plant Reprod 30(3):141–146. https://doi.org/10.1007/s00497-017-0304-3
Escobar Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, Grossniklaus U (2007) The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science 317(5838):656–660. https://doi.org/10.1126/science.1143562
Fedry J, Forcina J, Legrand P, Péhau-Arnaudet G, Haouz A, Johnson M, Rey FA, Krey T (2018) Evolutionary diversification of the HAP2 membrane insertion motifs to drive gamete fusion across eukaryotes. PLoS Biol 16(8):e2006357. https://doi.org/10.1371/journal.pbio.2006357
Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C (2016) Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife 5:e20542. https://doi.org/10.7554/eLife.20542
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. https://doi.org/10.1083/jcb.152.5.1019
Fédry J, Liu Y, Péhau-Arnaudet G, Pei J, Li W, Tortorici MA, Traincard F, Meola A, Bricogne G, Grishin NV, Snell WJ, Rey FA, Krey T (2017) The ancient gamete fusogen HAP2 is a eukaryotic class ii fusion protein. Cell 168(5):904–915.e910. https://doi.org/10.1016/j.cell.2017.01.024
Galen C (1999) Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. Bioscience 49(8):631–640. https://doi.org/10.2307/1313439
Galindo-Trigo S, Blanco-Tourinan N, DeFalco TA, Wells ES, Gray JE, Zipfel C, Smith LM (2019) CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception. EMBO Rep 21:e48466. https://doi.org/10.15252/embr.201948466
Garcia-Quiros E, Alche JD, Karpinska B, Foyer CH (2020) Glutathione redox state plays a key role in flower development and pollen vigour. J Exp Bot 71(2):730–741. https://doi.org/10.1093/jxb/erz376
Ge Z, Bergonci T, Zhao Y, Zou Y, Du S, Liu M-C, Luo X, Ruan H, García-Valencia LE, Zhong S, Hou S, Huang Q, Lai L, Moura DS, Gu H, Dong J, Wu H-M, Dresselhaus T, Xiao J, Cheung AY, Qu L-J (2017) Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358(6370):1596–1600. https://doi.org/10.1126/science.aao3642
Ge Z, Cheung AY, Qu LJ (2019a) Pollen tube integrity regulation in flowering plants: insights from molecular assemblies on the pollen tube surface. New Phytol 222(2):687–693. https://doi.org/10.1111/nph.15645
Ge Z, Zhao Y, Liu M-C, Zhou L-Z, Wang L, Zhong S, Hou S, Jiang J, Liu T, Huang Q, Xiao J, Gu H, Wu H-M, Dong J, Dresselhaus T, Cheung AY, Qu L-J (2019b) LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity. Curr Biol 29:1–10. https://doi.org/10.1016/j.cub.2019.08.032
George L, Romanowsky SM, Harper JF, Sharrock RA (2008) The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146(2):716–728. https://doi.org/10.1104/pp.107.108118
Goldman M, Goldberg R, Mariani C (1994) Female sterile tobacco plants are produced by stigma-specific cell ablation. EMBO J 13(13):2976–2984
Gremski K, Ditta G, Yanofsky MF (2007) The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 134(20):3593–3601. https://doi.org/10.1242/dev.011510
Grossniklaus U (2017) Polyspermy produces tri-parental seeds in maize. Curr Biol 27(24):R1300–R1302. https://doi.org/10.1016/j.cub.2017.10.059
Groß-Hardt R, Kägi C, Baumann N, Moore JM, Baskar R, Gagliano WB, Jürgens G, Grossniklaus U (2007) LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLoS Biol 5(3):e47. https://doi.org/10.1371/journal.pbio.0050047
Gu T, Mazzurco M, Sulaman W, Matias DD, Goring DR (1998) Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci 95(1):382–387. https://doi.org/10.1073/pnas.95.1.382
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. https://doi.org/10.1083/jcb.200409140
Gu Z, Li W, Doughty J, Meng D, Yang Q, Yuan H, Li Y, Chen Q, Yu J, Cs L, Li T (2019) A gamma-thionin protein from apple, MdD1, is required for defence against S-RNase-induced inhibition of pollen tube prior to self/non-self recognition. Plant Biotechnol. https://doi.org/10.1111/pbi.13131
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(2):528–533. https://doi.org/10.1104/pp.113.231274
Gunning BES, Pate JS (1969) “Transfer cells” Plant cells with wall ingrowths, specialized in relation to short distance transport of solutes—their occurrence, structure, and development. Protoplasma 68(1):107–133. https://doi.org/10.1007/bf01247900
Hamamura Y, Saito C, Awai C, Kurihara D, Miyawaki A, Nakagawa T, Kanaoka Masahiro M, Sasaki N, Nakano A, Berger F, Higashiyama T (2011) Live-cell imaging reveals the dynamics of two sperm cells during double fertilization in Arabidopsis thaliana. Curr Biol 21(6):497–502. https://doi.org/10.1016/j.cub.2011.02.013
Hao L, Liu J, Zhong S, Gu H, Qu L-J (2016) AtVPS41-mediated endocytic pathway is essential for pollen tube–stigma interaction in Arabidopsis. Proc Natl Acad Sci 113(22):6307–6312. https://doi.org/10.1073/pnas.1602757113
Hayashi K, Surani MA (2009) Resetting the epigenome beyond pluripotency in the germline. Cell Stem Cell 4(6):493–498. https://doi.org/10.1016/j.stem.2009.05.007
Heng HHQ (2009) The genome-centric concept: resynthesis of evolutionary theory. BioEssays 31(5):512–525. https://doi.org/10.1002/bies.200800182
Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Dev Biol 17(1):159–187. https://doi.org/10.1146/annurev.cellbio.17.1.159
Hernández-Lagana E, Rodríguez-Leal D, Lúa J, Vielle-Calzada J-P (2016) A multigenic network of ARGONAUTE4 clade members controls early megaspore formation in Arabidopsis. Genetics 204(3):1045–1056. https://doi.org/10.1534/genetics.116.188151
Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Ann Bot 41(176):1233–1258. https://doi.org/10.1093/oxfordjournals.aob.a085414
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(12):2019–2031. https://doi.org/10.1105/tpc.10.12.2019
Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima SY, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 293(5534):1480–1483. https://doi.org/10.1126/science.1062429
Hiscock SJ, Doughty J, Willis AC, Dickinson HG (1995) A 7-kDa pollen coating-borne peptide from Brassica napus interacts with S-locus glycoprotein and S-locus-related glycoprotein. Planta 196(2):367–374. https://doi.org/10.1007/bf00201397
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. https://doi.org/10.1105/tpc.9.11.1999
Hu X, Zhang Z, Li W, Fu Z, Zhang S, Xu P (2009) cDNA cloning and expression analysis of a putative decarbonylase TaCer1 from wheat (Triticum aestivum L.). Acta Physiol Plant 31(6):1111–1118. https://doi.org/10.1007/s11738-009-0329-9
Hu W, Liu Y, Loka DA, Zahoor R, Wang S, Zhou Z (2019) Drought limits pollen tube growth rate by altering carbohydrate metabolism in cotton (Gossypium hirsutum) pistils. Plant Sci 286:108–117. https://doi.org/10.1016/j.plantsci.2019.06.003
Hua Z, Kao T-h (2006) Identification and characterization of components of a putative Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18(10):2531–2553. https://doi.org/10.1105/tpc.106.041061
Huck N, Moore JM, Federer M, Grossniklaus U (2003) The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. Development 130(10):2149–2159. https://doi.org/10.1242/dev.00458
Hülskamp M, Kopczak SD, Horejsi TF, Kihl BK, Pruitt RE (1995a) Identification of genes required for pollen-stigma recognition in Arabidopsis thaliana. Plant J 8(5):703–714. https://doi.org/10.1046/j.1365-313X.1995.08050703.x
Hülskamp M, Schneitz K, Pruitt RE (1995b) Genetic evidence for a long-range activity that directs pollen tube guidance in Arabidopsis. Plant Cell 7(1):57–64. https://doi.org/10.1105/tpc.7.1.57
Irish V (2017) The ABC model of floral development. Curr Biol 27(17):R887–R890. https://doi.org/10.1016/j.cub.2017.03.045
Ishikawa M (1918) Studies on the embryo sac and fertilization in Oenothera. Ann Bot 32(126):279–317. https://doi.org/10.1093/oxfordjournals.aob.a089677
Iwano M, Shiba H, Miwa T, Che F-S, 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. https://doi.org/10.1104/pp.104.046961
Iwano M, Igarashi M, Tarutani Y, Kaothien-Nakayama P, Nakayama H, Moriyama H, Yakabe R, Entani T, Shimosato-Asano H, Ueki M, Tamiya G, Takayama S (2014) A Pollen coat–inducible autoinhibited Ca2+-ATPase expressed in stigmatic papilla cells is required for compatible pollination in the . Plant Cell 26(2):636–649. https://doi.org/10.1105/tpc.113.121350
Jauh GY, Lord EM (1995) Movement of the tube cell in the lily style in the absence of the pollen grain and the spent pollen tube. Sex Plant Reprod 8(3):168–172. https://doi.org/10.1007/bf00242262
Jensen WA (1965) The ultrastructure and histochemistry of the synergids of cotton. Am J Bot 52(3):238–256. https://doi.org/10.1002/j.1537-2197.1965.tb06781.x
Jiang L, Yang S-L, Xie L-F, Puah CS, Zhang X-Q, Yang W-C, 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(2):584–596. https://doi.org/10.1105/tpc.104.027631
Jiao H, Liu Q, Zhang H, Qi K, Liu Z, Wang P, Wu J, Zhang S (2019) PbrPCCP1 mediates the PbrTTS1 signaling to control pollen tube growth in pear. Plant Sci 289:110244. https://doi.org/10.1016/j.plantsci.2019.110244
Johnson MA, Harper JF, Palanivelu R (2019) A fruitful journey: pollen tube navigation from germination to fertilization. Annu Rev Plant Biol 70(1):809–837. https://doi.org/10.1146/annurev-arplant-050718-100133
Kanaoka MM, Kawano N, Matsubara Y, Susaki D, Okuda S, Sasaki N, Higashiyama T (2011) Identification and characterization of TcCRP1, a pollen tube attractant from Torenia concolor. Ann Bot 108(4):739–747. https://doi.org/10.1093/aob/mcr111
Kaneda M, van Oostende-Triplet C, Chebli Y, Testerink C, Bednarek SY, Geitmann A (2019) Plant AP180 N-terminal homolog proteins are involved in clathrin-dependent endocytosis during pollen tube growth in Arabidopsis thaliana. Plant Cell Physiol 60(6):1316–1330. https://doi.org/10.1093/pcp/pcz036
Kasahara RD, Portereiko MF, Sandaklie Nikolova L, Rabiger DS, Drews GN (2005) MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17(11):2981–2992. https://doi.org/10.1105/tpc.105.034603
Kasahara RD, Maruyama D, Hamamura Y, Sakakibara T, Twell D, Higashiyama T (2012) Fertilization recovery after defective sperm cell release in Arabidopsis. Curr Biol 22(12):1084–1089. https://doi.org/10.1016/j.cub.2012.03.069
Kasahara RD, Maruyama D, Higashiyama T (2013) Fertilization recovery system is dependent on the number of pollen grains for efficient reproduction in plants. Plant Signal Behav 8(4):e23690. https://doi.org/10.4161/psb.23690
Kasahara RD, Notaguchi M, Nagahara S, Suzuki T, Susaki D, Honma Y, Maruyama D, Higashiyama T (2016) Pollen tube contents initiate ovule enlargement and enhance seed coat development without fertilization. Sci Adv 2(10):e1600554. https://doi.org/10.1126/sciadv.1600554
Kemp BP, Doughty J (2007) S cysteine-rich (SCR) binding domain analysis of the Brassica self-incompatibility S-locus receptor kinase. New Phytol 175(4):619–629. https://doi.org/10.1111/j.1469-8137.2007.02126.x
Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, Panstruga R, Grossniklaus U (2010) Conserved molecular components for pollen tube reception and fungal invasion. Science 330(6006):968–971. https://doi.org/10.1126/science.1195211
Kim S, Mollet J-C, Dong J, Zhang K, Park S-Y, Lord EM (2003) Chemocyanin, a small basic protein from the lily stigma, induces pollen tube chemotropism. Proc Natl Acad Sci USA 100(26):16125–16130. https://doi.org/10.1073/pnas.2533800100
Kim SS, Grienenberger E, Lallemand B, Colpitts CC, Kim SY, Souza CdA, Geoffroy P, Heintz D, Krahn D, Kaiser M, Kombrink E, Heitz T, Suh D-Y, Legrand M, Douglas CJ (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl α-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 22(12):4045–4066. https://doi.org/10.1105/tpc.110.080028
Knowles AF (2011) The GDA1_CD39 superfamily: NTPDases with diverse functions. Purinergic Signal 7(1):21–45. https://doi.org/10.1007/s11302-010-9214-7s
Koornneef M, Hanhart C, Thiel F (1989) A genetic and phenotypic description of eceriferum (cer) mutants in Arabidopsis thaliana. J Hered 80(2):118–122
Laggoun F, Dardelle F, Dehors J, Falconet D, Driouich A, Rochais C, Dallemagne P, Lehner A, Mollet J-C (2019) A chemical screen identifies two novel small compounds that alter Arabidopsis thaliana pollen tube growth. hBMC Plant Biol 19(1):152. https://doi.org/10.1186/s12870-019-1743-9
Lausser A, Kliwer I, Srilunchang K-O, Dresselhaus T (2009) Sporophytic control of pollen tube growth and guidance in maize. J Exp Bot 61(3):673–682. https://doi.org/10.1093/jxb/erp330
Lee CB, Swatek KN, McClure B (2008) Pollen proteins bind to the C-terminal domain of Nicotiana alata pistil arabinogalactan proteins. J Biol Chem 283(40):26965–26973. https://doi.org/10.1074/jbc.M804410200
Lee SK, Kim H, Cho JI, Nguyen CD, Moon S, Park JE, Park HR, Huh JH, Jung KH, Guiderdoni E, Jeon JS (2020) Deficiency of rice hexokinase HXK5 impairs synthesis and utilization of starch in pollen grains and causes male sterility. J Exp Bot 71(1):116–125. https://doi.org/10.1093/jxb/erz436
Leroux C, Bouton S, Kiefer-Meyer M-C, Fabrice TN, Mareck A, Guénin S, Fournet F, Ringli C, Pelloux J, Driouich A, Lerouge P, Lehner A, Mollet J-C (2015) PECTIN METHYLESTERASE48 is involved in Arabidopsis pollen grain germination. Plant Physiol 167(2):367–380. https://doi.org/10.1104/pp.114.250928
Leszczuk A, Kozioł A, Szczuka E, Zdunek A (2019) Analysis of AGP contribution to the dynamic assembly and mechanical properties of cell wall during pollen tube growth. Plant Sci 281:9–18. https://doi.org/10.1016/j.plantsci.2019.01.005
Leydon AR, Beale Kristin M, Woroniecka K, Castner E, Chen J, Horgan C, Palanivelu R, Johnson MA (2013) Three MYB transcription factors control pollen tube differentiation required for sperm release. Curr Biol 23(13):1209–1214. https://doi.org/10.1016/j.cub.2013.05.021
Leydon AR, Tsukamoto T, Dunatunga D, Qin Y, Johnson MA, Palanivelu R (2015) Pollen tube discharge completes the process of synergid degeneration that is initiated by pollen tube-synergid interaction in Arabidopsis. Plant Physiol 169(1):485–496. https://doi.org/10.1104/pp.15.00528
Li YQ, Chen F, Linskens HF, Cresti M (1994) Distribution of unesterified and esterified pectins in cell walls of pollen tubes of flowering plants. Sex Plant Reprod 7(3):145–152. https://doi.org/10.1007/bf00228487
Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11(9):1731–1742. https://doi.org/10.1105/tpc.11.9.1731
Li S, Ge F-R, Xu M, Zhao X-Y, Huang G-Q, Zhou L-Z, Wang J-G, 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(3):486–497. https://doi.org/10.1111/tpj.12139
Li C, Yeh FL, Cheung AY, Duan Q, Kita D, Liu MC, Maman J, Luu EJ, Wu BW, Gates L, Jalal M, Kwong A, Carpenter H, Wu H-M (2015a) Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4:e06587. https://doi.org/10.7554/eLife.06587
Li HJ, Zhu SS, Zhang MX, Wang T, Liang L, Xue Y, Shi DQ, Liu J, Yang WC (2015b) Arabidopsis CBP1 is a novel regulator of transcription initiation in central cell-mediated pollen tube guidance. Plant Cell 27(10):2880–2893. https://doi.org/10.1105/tpc.15.00370
Li CL, Meng D, Pineros MA, Mao Y, Dandekar AM, Cheng L (2019) A sugar transporter takes up both hexose and sucrose for sorbitol-modulated in vitro pollen tube growth in apple. Plant Cell. https://doi.org/10.1105/tpc.19.00638
Liang Y, Tan Z-M, Zhu L, Niu Q-K, Zhou J-J, Li M, Chen L-Q, Zhang X-Q, Ye D (2013) MYB97, MYB101 and MYB120 function as male factors that control pollen tube-synergid interaction in Arabidopsis thaliana fertilization. PLoS Genet 9(11):e1003933. https://doi.org/10.1371/journal.pgen.1003933
Lin S-Y, Chen P-W, Chuang M-H, Juntawong P, Bailey-Serres J, Jauh G-Y (2014) Profiling of translatomes of in vivo-grown pollen tubes reveals genes with roles in micropylar guidance during pollination in Arabidopsis. Plant Cell 26(2):602–618. https://doi.org/10.1105/tpc.113.121335
Lindner H, Kessler SA, Müller LM, Shimosato-Asano H, Boisson-Dernier A, Grossniklaus U (2015) TURAN and EVAN mediate pollen tube reception in Arabidopsis synergids through protein glycosylation. PLoS Biol 13(4):e1002139. https://doi.org/10.1371/journal.pbio.1002139
Liu Y, Zhang S (2004) Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16(12):3386–3399. https://doi.org/10.1105/tpc.104.026609
Liu J, Zhong S, Guo X, Hao L, Wei X, Huang Q, Hou Y, Shi J, Wang C, Gu H, Qu L-J (2013) Membrane-bound RLCKs LIP1 and LIP2 are essential male factors controlling male-female attraction in Arabidopsis. Curr Biol 23(11):993–998. https://doi.org/10.1016/j.cub.2013.04.043
Liu J, Zhang H, Lian X, Converse R, Zhu L (2016) Identification of interacting motifs between armadillo repeat containing 1 (ARC1) and Exocyst 70 A1 (Exo70A1) proteins in Brassica oleracea. Protein J 35(1):34–43. https://doi.org/10.1007/s10930-015-9644-8
Liu C, Xin Y, Xu L, Cai Z, Xue Y, Liu Y, Xie D, Liu Y, Qi Y (2018) Arabidopsis ARGONAUTE 1 binds chromatin to promote gene transcription in response to hormones and stresses. Dev Cell 44(3):348–361.e347. https://doi.org/10.1016/j.devcel.2017.12.002
Liu X, Adhikari PB, Kasahara RD (2019) Pollen tube contents from failed fertilization contribute to seed coat initiation in Arabidopsis. F1000Research 8(348):348. https://doi.org/10.12688/f1000research.18644.2
Liu L, Zhao L, Chen P, Cai H, Hou Z, Jin X, Aslam M, Chai M, Lai L, He Q, Liu Y, Huang X, Chen H, Chen Y, Qin Y (2020) ATP binding cassette transporters ABCG1 and ABCG16 affect reproductive development via auxin signaling in Arabidopsis. Plant J. https://doi.org/10.1111/tpj.14690
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(1):81–93. https://doi.org/10.1105/tpc.110.080499
Luu D-T, Heizmann P, Dumas C, Trick M, Cappadocia M (1997) Involvement of SLR1 genes in pollen adhesion to the stigmatic surface in Brassicaceae. Sex Plant Reprod 10(4):227–235. https://doi.org/10.1007/s004970050091
Luu D-T, Marty-Mazars D, Trick M, Dumas C, Heizmann P (1999) Pollen–stigma adhesion in Brassica spp. involves SLG and SLR1 glycoproteins. Plant Cell 11(2):251–262. https://doi.org/10.1105/tpc.11.2.251
Ma L, Xu X, Cui S, Sun DJCSB (1998) Effects of extracellular calmodulin on pollen germination and tube growth. Chin Sci Bull 43(2):143–146. https://doi.org/10.1007/bf02883929
Malho R, Trewavas AJ (1996) Localized apical increases of cytosolic free calcium control pollen tube orientation. Plant Cell 8(11):1935–1949. https://doi.org/10.1105/tpc.8.11.1935
Mandel MA, Bowman JL, Kempin SA, Ma H, Meyerowitz EM, Yanofsky MF (1992) Manipulation of flower structure in transgenic tobacco. Cell 71(1):133–143. https://doi.org/10.1016/0092-8674(92)90272-E
Márton ML, Cordts S, Broadhvest J, Dresselhaus T (2005) Micropylar pollen tube guidance by Egg Apparatus 1 of maize. Science 307(5709):573–576. https://doi.org/10.1126/science.1104954
Márton ML, Fastner A, Uebler S, Dresselhaus T (2012) Overcoming hybridization barriers by the secretion of the maize pollen tube attractant ZmEA1 from Arabidopsis ovules. Curr Biol 22(13):1194–1198. https://doi.org/10.1016/j.cub.2012.04.061
Maruyama D, Hamamura Y, Takeuchi H, Susaki D, Nishimaki M, Kurihara D, Kasahara Ryushiro D, Higashiyama T (2013) Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev Cell 25(3):317–323. https://doi.org/10.1016/j.devcel.2013.03.013
Maruyama D, Völz R, Takeuchi H, Mori T, Igawa T, Kurihara D, Kawashima T, Ueda M, Ito M, Umeda M, Nishikawa S-i, Groß-Hardt R, Higashiyama T (2015) Rapid elimination of the persistent synergid through a cell fusion mechanism. Cell 161(4):907–918. https://doi.org/10.1016/j.cell.2015.03.018
McCourt RM, Delwiche CF, Karol KG (2004) Charophyte algae and land plant origins. Trends Ecol Evol 19(12):661–666. https://doi.org/10.1016/j.tree.2004.09.013
McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signalling crosstalk? New Phytol 172(2):221–228. https://doi.org/10.1111/j.1469-8137.2006.01875.x
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(6370):1600–1603. https://doi.org/10.1126/science.aao5467
Meng J-G, Zhang M-X, Yang W-C, Li H-J (2019) TICKET attracts pollen tubes and mediates reproductive isolation between relative species in Brassicaceae. Sci China Life Sci 62(11):1413–1419. https://doi.org/10.1007/s11427-019-9833-3
Messerli MA, Robinson KR (1998) Cytoplasmic acidification and current influx follow growth pulses of Lilium longiflorum pollen tubes. Plant J 16(1):87–91. https://doi.org/10.1046/j.1365-313x.1998.00266.x
Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu L-H, Obermeyer G, Feijó JA (2011) Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332(6028):434–437. https://doi.org/10.1126/science.1201101
Minnaar C, de Jager ML, Anderson B (2019) Intraspecific divergence in floral-tube length promotes asymmetric pollen movement and reproductive isolation. New Phytol 224(3):1160–1170. https://doi.org/10.1111/nph.15971
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(15):1327–1331. https://doi.org/10.1016/j.cub.2009.06.064
Mizukami Akane G, 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(8):1091–1097. https://doi.org/10.1016/j.cub.2016.02.040
Mizuta Y, Higashiyama T (2018) Chemical signaling for pollen tube guidance at a glance. J Cell Sci. https://doi.org/10.1242/jcs.208447
Mogensen HL (1978) Pollen tube-synergid interactions in Proboscidea louisianica (Martineaceae). Am J Bot 65(9):953–964. https://doi.org/10.2307/2442682
Mori T, Kuroiwa H, Higashiyama T, Kuroiwa T (2005) GENERATIVE CELL SPECIFIC 1 is essential for angiosperm fertilization. Nat Cell Biol 8:64. https://doi.org/10.1038/ncb1345
Mori T, Hirai M, Kuroiwa T, Miyagishima S-Y (2011) The functional domain of GCS1-based gamete fusion resides in the amino terminus in plant and parasite species. PLoS ONE 5(12):e15957. https://doi.org/10.1371/journal.pone.0015957
Mori T, Igawa T, Tamiya G, Miyagishima S-Y, Berger F (2014) Gamete attachment requires GEX2 for successful fertilization in Arabidopsis. Curr Biol 24(2):170–175. https://doi.org/10.1016/j.cub.2013.11.030
Mulcahy GB, Mulcahy DL (1987) Induced pollen tube directionality. Am J Bot 74(9):1458–1459. https://doi.org/10.1002/j.1537-2197.1987.tb08759.x
Muro K, Matsuura-Tokita K, Tsukamoto R, Kanaoka MM, Ebine K, Higashiyama T, Nakano A, Ueda T (2018) ANTH domain-containing proteins are required for the pollen tube plasma membrane integrity via recycling ANXUR kinases. Commun Biol 1:152–152. https://doi.org/10.1038/s42003-018-0158-8
Nagahara S, Takeuchi H, Higashiyama T (2015) Generation of a homozygous fertilization-defective gcs1 mutant by heat-inducible removal of a rescue gene. Plant Reprod 28(1):33–46. https://doi.org/10.1007/s00497-015-0256-4
Nakel T, Tekleyohans DG, Mao Y, Fuchert G, Vo D, Groß-Hardt R (2017) Triparental plants provide direct evidence for polyspermy induced polyploidy. Nat Commun 8(1):1033. https://doi.org/10.1038/s41467-017-01044-y
Nasrallah JB (2019) Self-incompatibility in the Brassicaceae: regulation and mechanism of self-recognition. In: Grossniklaus U (ed) Current topics in developmental biology, vol 131. Academic Press, Cambridge, pp 435–452
Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signalling molecules in plants. J Exp Bot 53(372):1237–1247. https://doi.org/10.1093/jexbot/53.372.1237
Ngugi HK, Scherm H (2004) Pollen mimicry during infection of blueberry flowers by conidia of Monilinia vaccinii-corymbosi. Physiol Mol Plant Pathol 64(3):113–123. https://doi.org/10.1016/j.pmpp.2004.08.004
Niedojadlo K, Kupiecka M, Kolowerzo-Lubnau A, Lenartowski R, Niedojadlo J, Bednarska-Kozakiewicz E (2020) Dynamic distribution of ARGONAUTE1 (AGO1) and ARGONAUTE4 (AGO4) in Hyacinthusorientalis L. pollen grains and pollen tubes growing in vitro. Protoplasma. https://doi.org/10.1007/s00709-019-01463-2
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. https://doi.org/10.1038/nature07882
Otto S (2008) Sexual reproduction and the evolution of sex. Nat Educ 1:1
O’Brien M, Major G, Chantha S-C, Matton DP (2004) Isolation of S-RNase binding proteins from Solanum chacoense: identification of an SBP1 (RING finger protein) orthologue. Sex Plant Reprod 17(2):81–87. https://doi.org/10.1007/s00497-004-0218-8
Palanivelu R, Preuss D (2006) Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol 6(1):7. https://doi.org/10.1186/1471-2229-6-7
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(1):47–59. https://doi.org/10.1016/S0092-8674(03)00479-3
Pasqualini S, Cresti M, Del Casino C, Faleri C, Frenguelli G, Tedeschini E, Ederli L (2015) Roles for NO and ROS signalling in pollen germination and pollen-tube elongation in Cupressus arizonica. Biol Plant 59(4):735–744. https://doi.org/10.1007/s10535-015-0538-6
Paxson-Sowders DM, Owen HA, Makaroff CA (1997) A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma 198(1):53–65. https://doi.org/10.1007/bf01282131
Paxson-Sowders DM, Dodrill CH, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127(4):1739–1749. https://doi.org/10.1104/pp.010517
Pearce G, Yamaguchi Y, Munske G, Ryan CA (2010) Structure-activity studies of RALF, rapid alkalinization factor, reveal an essential—YISY—motif. Peptides 31(11):1973–1977. https://doi.org/10.1016/j.peptides.2010.08.012
Pereira AM, Nobre MS, Pinto SC, Lopes AL, Costa ML, Masiero S, Coimbra S (2016) “Love is strong, and you're so sweet”: Jagger is essential for persistent synergid degeneration and polytubey block in Arabidopsis thaliana. Molecular Plant 9(4):601–614. https://doi.org/10.1016/j.molp.2016.01.002
Potocký M, Eliáš M, Profotová B, Novotná Z, Valentová O, Žárský V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217(1):122–130. https://doi.org/10.1007/s00425-002-0965-4
Potocký M, Jones MA, Bezvoda R, Smirnoff N, Žárský V (2007) Reactive oxygen species produced by NADPH oxidase are involved in pollen tube growth. New Phytol 174(4):742–751. https://doi.org/10.1111/j.1469-8137.2007.02042.x
Pozzi FI, Pratta GR, Acuña CA, Felitti SA (2019) Xenia in bahiagrass: gene expression at initial seed formation. Seed Sci Res 29(1):29–37. https://doi.org/10.1017/S0960258518000375
Prado AM, Porterfield DM, Feijó JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131(11):2707–2714. https://doi.org/10.1242/dev.01153
Punwani JA, Rabiger DS, Drews GN (2007) MYB98 positively regulates a battery of synergid-expressed genes encoding filiform apparatus–localized proteins. Plant Cell 19(8):2557–2568. https://doi.org/10.1105/tpc.107.052076
Pérez DGJA, Barberini ML, Amodeo G, Muschietti JP (2016) Pollen aquaporins: what are they there for? Plant Signal Behav 11(9):e1217375–e1217375. https://doi.org/10.1080/15592324.2016.1217375
Qin Y, Leydon AR, Manziello A, Pandey R, Mount D, Denic S, Vasic B, Johnson MA, Palanivelu R (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet 5(8):e1000621. https://doi.org/10.1371/journal.pgen.1000621
Quilichini TD, Friedmann MC, Samuels AL, Douglas CJ (2010) ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol 154(2):678–690. https://doi.org/10.1104/pp.110.161968
Rademacher S, Sprunck S (2013) Downregulation of egg cell-secreted EC1 is accompanied with delayed gamete fusion and polytubey. Plant Signal Behav 8(12):e27377. https://doi.org/10.4161/psb.27377
Reichler SA, Torres J, Rivera AL, Cintolesi VA, Clark G, Roux SJ (2009) Intersection of two signalling pathways: extracellular nucleotides regulate pollen germination and pollen tube growth via nitric oxide. J Exp Bot 60(7):2129–2138. https://doi.org/10.1093/jxb/erp091
Rejón JD, Delalande F, Schaeffer-Reiss C, Carapito C, Zienkiewicz K, de Dios AJ, Rodríguez-García MI, Van Dorsselaer A, Castro AJ (2013) Proteomics profiling reveals novel proteins and functions of the plant stigma exudate. J Exp Bot 64(18):5695–5705. https://doi.org/10.1093/jxb/ert345
Roshchina VV, Mel'nikova EV (2001) Pollen chemosensitivity to ozone and peroxides. Russ J Plant Physiol 48(1):74–83. https://doi.org/10.1023/a:1009054732411
Roszak P, Köhler C (2011) Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc Natl Acad Sci 108(51):20826–20831. https://doi.org/10.1073/pnas.1117111108
Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure J-E (2003) Female control of male gamete delivery during fertilization in Arabidopsis thaliana. Curr Biol 13(5):432–436. https://doi.org/10.1016/S0960-9822(03)00093-9
Rottmann T, Fritz C, Sauer N, Stadler R (2018) Glucose uptake via STP transporters inhibits in vitro pollen tube growth in a HEXOKINASE1-dependent manner in Arabidopsis thaliana. Plant Cell 30(9):2057–2081. https://doi.org/10.1105/tpc.18.00356
Rounds CM, Bezanilla M (2013) Growth mechanisms in tip-growing plant cells. Annu Rev Plant Biol 64(1):243–265. https://doi.org/10.1146/annurev-arplant-050312-120150
Rozier F, Riglet L, Kodera C, Bayle V, Durand E, Schnabel J, Gaude T, Fobis-Loisy I (2020) Live-cell imaging of early events following pollen perception in self-incompatible Arabidopsis thaliana. J Exp Bot. https://doi.org/10.1093/jxb/eraa008
Safavian D, Goring DR (2013) Secretory activity is rapidly induced in stigmatic papillae by compatible pollen, but inhibited for self-incompatible pollen in the Brassicaceae. PLoS ONE 8(12):e84286. https://doi.org/10.1371/journal.pone.0084286
Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL, Goring DR (2009) Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21(9):2655–2671. https://doi.org/10.1105/tpc.109.069740
Sandfaer J (1979) Frequency of aneuploids in progenies of autotriploid barley, Hordeum vulgare L. Hereditas 90(2):213–217. https://doi.org/10.1111/j.1601-5223.1979.tb01308.x
Sato R, Maeshima M (2019) The ER-localized aquaporin SIP2;1 is involved in pollen germination and pollen tube elongation in Arabidopsis thaliana. Plant Mol Biol 100(3):335–349. https://doi.org/10.1007/s11103-019-00865-3
Schierup MH, Mable BK, Awadalla P, Charlesworth D (2001) Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics 158(1):387–399
Schiøtt M, Romanowsky SM, Bækgaard 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(25):9502–9507. https://doi.org/10.1073/pnas.0401542101
Shimizu KK, Okada K (2000) Attractive and repulsive interactions between female and male gametophytes in Arabidopsis pollen tube guidance. Development 127(20):4511–4518. https://doi.org/10.5167/uzh-71801
Shimosato H, Yokota N, Shiba H, Iwano M, Entani T, Che F-S, Watanabe M, Isogai A, Takayama S (2007) Characterization of the SP11/SCR high-affinity binding site involved in self/nonself recognition in Brassica self-incompatibility. Plant Cell 19(1):107–117. https://doi.org/10.1105/tpc.105.038869
Sims TL, Ordanic M (2001) Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol 47(6):771–783. https://doi.org/10.1023/a:1013639528858
Šírová J, Sedlářová M, Piterková J, Luhová L, Petřivalský M (2011) The role of nitric oxide in the germination of plant seeds and pollen. Plant Sci 181(5):560–572. https://doi.org/10.1016/j.plantsci.2011.03.014
Smith DK, Jones DM, Lau JBR, Cruz ER, Brown E, Harper JF, Wallace IS (2018) A putative protein O-fucosyltransferase facilitates pollen tube penetration through the stigma–style interface. Plant Physiol 176(4):2804–2818. https://doi.org/10.1104/pp.17.01577
Sprunck S, Rademacher S, Vogler F, Gheyselinck J, Grossniklaus U, Dresselhaus T (2012) Egg cell-secreted EC1 triggers sperm cell activation during double fertilization. Science 338(6110):1093–1097. https://doi.org/10.1126/science.1223944
Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci 88(19):8816–8820. https://doi.org/10.1073/pnas.88.19.8816
Steinebrunner I, Wu J, Sun Y, Corbett A, Roux SJ (2003) Disruption of apyrases inhibits pollen germination in Arabidopsis. Plant Physiol 4:1638–1647. https://doi.org/10.1104/pp.102.014308
Steinhorst L, Kudla J (2013) Calcium: a central regulator of pollen germination and tube growth. Biochim Biophys Acta 1833(7):1573–1581. https://doi.org/10.1016/j.bbamcr.2012.10.009
Stone SL, Anderson EM, Mullen RT, Goring DR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15(4):885–898. https://doi.org/10.1105/tpc.009845
Strasburger E (1877) Über befruchtung und zelltheilung. A. Abel, Binghamto
Stührwohldt N, Dahlke RI, Kutschmar A, Peng X, Sun M-X, Sauter M (2015) Phytosulfokine peptide signaling controls pollen tube growth and funicular pollen tube guidance in Arabidopsis thaliana. Physiol Plant 153(4):643–653. https://doi.org/10.1111/ppl.12270
Suzuki T, Masaoka K, Nishi M, Nakamura K, Ishiguro S (2008) Identification of kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana. Plant Cell Physiol 49(10):1465–1477. https://doi.org/10.1093/pcp/pcn131
Swanson R, Clark T, Preuss D (2005) Expression profiling of Arabidopsis stigma tissue identifies stigma-specific genes. Sex Plant Reprod 18(4):163–171. https://doi.org/10.1007/s00497-005-0009-x
Takahashi T, Mori T, Ueda K, Yamada L, Nagahara S, Higashiyama T, Sawada H, Igawa T (2018) The male gamete membrane protein DMP9/DAU2 is required for double fertilization in flowering plants. Development 145(23):dev170076. https://doi.org/10.1242/dev.170076
Takayama S, Shiba H, Iwano M, Asano K, Hara M, Che F-S, Watanabe M, Hinata K, Isogai A (2000) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen–stigma adhesion. Proc Natl Acad Sci 97(7):3765–3770. https://doi.org/10.1073/pnas.97.7.3765
Takemoto K, Ebine K, Askani JC, Krüger F, Gonzalez ZA, Ito E, Goh T, Schumacher K, Nakano A, Ueda T (2018) Distinct sets of tethering complexes, SNARE complexes, and Rab GTPases mediate membrane fusion at the vacuole in Arabidopsis. Proc Natl Acad Sci 115(10):E2457–E2466. https://doi.org/10.1073/pnas.1717839115
Takeuchi H, Higashiyama T (2012) A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. PLoS Biol 10(12):e1001449. https://doi.org/10.1371/journal.pbio.1001449
Takeuchi H, Higashiyama T (2016) Tip-localized receptors control pollen tube growth and LURE sensing in Arabidopsis. Nature 531:245. https://doi.org/10.1038/nature17413
Terrile MC, París R, Calderón-Villalobos LIA, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70(3):492–500. https://doi.org/10.1111/j.1365-313X.2011.04885.x
Theißen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143(18):3259–3271. https://doi.org/10.1242/dev.134080
Tian G-W, Chen M-H, Zaltsman A, Citovsky V (2006) Pollen-specific pectin methylesterase involved in pollen tube growth. Dev Biol 294(1):83–91. https://doi.org/10.1016/j.ydbio.2006.02.026
Tian C, Shi Q, Cui X, Guo J, Yang Z, Shi J (2019) Spatiotemporal dynamics of a reaction-diffusion model of pollen tube tip growth. J Math Biol 79(4):1319–1355. https://doi.org/10.1007/s00285-019-01396-7
Tirlapur UK, Willemse MTM (1992) Changes in calcium and calmodulin levels during microsporogenesis, pollen development and germination in Gasteria verrucosa (Mill.) H. Duval. Sex Plant Reprod 5(3):214–223. https://doi.org/10.1007/bf00189814
Toda E, Okamoto T (2019) Polyspermy in angiosperms: its contribution to polyploid formation and speciation. Mol Reprod Dev. https://doi.org/10.1002/mrd.23295
Twell D (2011) Male gametogenesis and germline specification in flowering plants. Sex Plant Reprod 24(2):149–160. https://doi.org/10.1007/s00497-010-0157-5
Vaz Dias F, Serrazina S, Vitorino M, Marchese D, Heilmann I, Godinho M, Rodrigues M, Malhó R (2019) A role for diacylglycerol kinase 4 in signalling crosstalk during Arabidopsis pollen tube growth. New Phytol 222(3):1434–1446. https://doi.org/10.1111/nph.15674
Vogler H, Santos-Fernandez G, Mecchia MA, Grossniklaus U (2019) To preserve or to destroy, that is the question: the role of the cell wall integrity pathway in pollen tube growth. Curr Opin Plant Biol 52:131–139. https://doi.org/10.1016/j.pbi.2019.09.002
von Besser K, Frank AC, Johnson MA, Preuss D (2006) Arabidopsis HAP2 (GCS1) is a sperm-specific gene required for pollen tube guidance and fertilization. Development 133(23):4761–4769. https://doi.org/10.1242/dev.02683
Wang J, Higgins VJ (2005) Nitric oxide modulates H2O2-mediated defenses in the Colletotrichum coccodes-tomato interaction. Physiol Mol Plant Pathol 67(3):131–137. https://doi.org/10.1016/j.pmpp.2005.11.002
Wang H, Liu Y, Bruffett K, Lee J, Hause G, Walker JC, Zhang S (2008a) Haplo-insufficiency of MPK3 in MPK6 mutant background uncovers a novel function of these two mapks in Arabidopsis ovule development. Plant Cell 20(3):602–613. https://doi.org/10.1105/tpc.108.058032
Wang Y, Zhang W-Z, Song L-F, Zou J-J, Su Z, Wu W-H (2008b) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148(3):1201–1211. https://doi.org/10.1104/pp.108.126375
Wang W-Y, Zhang L, Xing S, Ma Z, Liu J, Gu H, Qin G, Qu L-J (2012) Arabidopsis AtVPS15 plays essential roles in pollen germination possibly by interacting with AtVPS34. J Genet Genom 39(2):81–92. https://doi.org/10.1016/j.jgg.2012.01.002
Wang L, Lv X, Li H, Zhang M, Wang H, Jin B, Chen T (2013) Inhibition of apoplastic calmodulin impairs calcium homeostasis and cell wall modeling during Cedrus deodara pollen tube growth. PLoS ONE 8(2):e55411. https://doi.org/10.1371/journal.pone.0055411
Wang T, Liang L, Xue Y, Jia PF, Chen W, Zhang MX, Wang YC, Li HJ, Yang WC (2016) A receptor heteromer mediates the male perception of female attractants in plants. Nature 531:241. https://doi.org/10.1038/nature16975
Wang L, Clarke LA, Eason RJ, Parker CC, Qi B, Scott RJ, Doughty J (2017) PCP-B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen–stigma interactions. New Phytol 213(2):764–777. https://doi.org/10.1111/nph.14162
Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392(6678):818–821. https://doi.org/10.1038/33929
Wong JL, Leydon AR, Johnson MA (2010) HAP2(GCS1)-dependent gamete fusion requires a positively charged carboxy-terminal domain. PLoS Genet 6(3):e1000882. https://doi.org/10.1371/journal.pgen.1000882
Wu H-m, Wang H, Cheung AY (1995) A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82(3):395–403. https://doi.org/10.1016/0092-8674(95)90428-X
Wu J, Qin Y, Zhao J (2008) Pollen tube growth is affected by exogenous hormones and correlated with hormone changes in styles in Torenia fournieri L. Plant Growth Regul 55(2):137–148. https://doi.org/10.1007/s10725-008-9268-5
Wu J, Steinebrunner I, Sun Y, Butterfield T, Torres J, Arnold D, Gonzalez A, Jacob F, Reichler S, Roux SJ (2007) Apyrases (nucleoside triphosphate-diphosphohydrolases) play a key role in growth control in Arabidopsis. Plant Physiol 144(2):961–975. https://doi.org/10.1104/pp.107.097568
Wudick MM, Luu D-T, Tournaire-Roux C, Sakamoto W, Maurel C (2014) Vegetative and sperm cell-specific aquaporins of Arabidopsis highlight the vacuolar equipment of pollen and contribute to plant reproduction. Plant Physiol 164(4):1697–1706. https://doi.org/10.1104/pp.113.228700
Xiao Y, Stegmann M, Han Z, DeFalco TA, Parys K, Xu L, Belkhadir Y, Zipfel C, Chai J (2019) Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572(7768):270–274. https://doi.org/10.1038/s41586-019-1409-7
Xu N, Gao X-Q, Zhao XY, Zhu DZ, Zhou LZ, Zhang XS (2011) Arabidopsis AtVPS15 is essential for pollen development and germination through modulating phosphatidylinositol 3-phosphate formation. Plant Mol Biol 77(3):251. https://doi.org/10.1007/s11103-011-9806-9
Yadegari R, Drews GN (2004) Female gametophyte development. Plant Cell 16(Suppl 1):S133–S141. https://doi.org/10.1105/tpc.018192
Yan A, Xu G, Yang Z-B (2009) Calcium participates in feedback regulation of the oscillating ROP1 Rho GTPase in pollen tubes. Proc Natl Acad Sci 106(51):22002–22007. https://doi.org/10.1073/pnas.0910811106
Yang WC, Shi DQ, Chen YH (2010) Female gametophyte development in flowering plants. Annu Rev Plant Biol 61(1):89–108. https://doi.org/10.1146/annurev-arplant-042809-112203
Yang K, Zang H-C, Converse R, Zhu L-Q, Yang Y-J, Xue L-Y, Luo B, Chang D-L, Gao Q-G, Wang X-J (2012) Interaction between two self-incompatible signal elements, EXO70A1 and ARC1. Acta Agron Sin 37(12):2136–2144. https://doi.org/10.1016/S1875-2780(11)60054-0
Yu B, Liu L, Wang T (2019) Deficiency of very long chain alkanes biosynthesis causes humidity-sensitive male sterility via affecting pollen adhesion and hydration in rice. Plant Cell Environ. https://doi.org/10.1111/pce.13637
Zhang S, Klessig DF (2001) MAPK cascades in plant defense signaling. Trends Plant Sci 6(11):520–527. https://doi.org/10.1016/S1360-1385(01)02103-3
Zhang Y, Li S, Zhou L-Z, Fox E, Pao J, Sun W, Zhou C, McCormick S (2011) Overexpression of Arabidopsis thaliana PTEN caused accumulation of autophagic bodies in pollen tubes by disrupting phosphatidylinositol 3-phosphate dynamics. Plant J 68(6):1081–1092. https://doi.org/10.1111/j.1365-313X.2011.04761.x
Zhong S, Liu M, Wang Z, Huang Q, Hou S, Xu Y-C, Ge Z, Song Z, Huang J, Qiu X, Shi Y, Xiao J, Liu P, Guo Y-L, Dong J, Dresselhaus T, Gu H, Qu L-J (2019) Cysteine-rich peptides promote interspecific genetic isolation in Arabidopsis. Science 364(6443):9564. https://doi.org/10.1126/science.aau9564
Zhou L-Z, Dresselhaus T (2019) Friend or foe: signaling mechanisms during double fertilization in flowering seed plants. In: Grossniklaus U (ed) Current topics in developmental biology, vol 131. Academic Press, Cambridge, pp 453–496
Zhou C, Yang H (1981) In vitro embryogenes in unfertilized embryo sacs of Oryza sativa L. Acta Bot Sin
Zhu L, Chu L-C, Liang Y, Zhang X-Q, Chen L-Q, Ye D (2018) The Arabidopsis CrRLK1L protein kinases BUPS1 and BUPS2 are required for normal growth of pollen tubes in the pistil. Plant J 95(3):474–486. https://doi.org/10.1111/tpj.13963
Zimmer C (2009) On the origin of sexual reproduction. Science 324(5932):1254–1256. https://doi.org/10.1126/science.324_1254
Zinkl GM, Preuss D (2000) Dissecting Arabidopsis pollen-stigma interactions reveals novel mechanisms that confer mating specificity. Ann Bot 85(suppl_1):15–21. https://doi.org/10.1006/anbo.1999.1066
Zinkl GM, Zwiebel BI, Grier DG, Preuss D (1999) Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 126(23):5431–5440
Funding
This work was supported by start-up funds from the School of Life Sciences, Fujian Agriculture and Forestry University (Grant #:114-712018008) and the FAFU-UCR Joint Center, Haixia Institute of Science and Technology, Fujian Agriculture and Forestry University. This work was also supported by Chinese NSFC fund, Grant Number 31970809. This work was also supported by the Precursory Research for Embryonic Science and Technology (grant 13416724 to R.D.K.; Kasahara Sakigake Project), Japan Science and Technology Agency.
Author information
Authors and Affiliations
Contributions
PBA and RDK designed the manuscript; LXY, SWZ, and WXY carried out the in vivo and semi in vitro pollen tube guidance experiments under the guidance of PBA; PBA prepared the figures and manuscript; and RDK guided and assisted during the manuscript preparation and revision.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Adhikari, P.B., Liu, X., Wu, X. et al. Fertilization in flowering plants: an odyssey of sperm cell delivery. Plant Mol Biol 103, 9–32 (2020). https://doi.org/10.1007/s11103-020-00987-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11103-020-00987-z