Abstract
Putrescine, spermine, and spermidine are among the most significant polyamines for plant growth and development, including pollen tube elongation. Although the effects of putrescine and spermine are well-known on tube elongation, little is known about the impact of spermidine. The aim of this study is to reveal how exogenic spermidine impinges positively and negatively on the factors involved in tube elongation such as actin cytoskeleton organization, calcium, pH and reactive oxygen species gradients, sucrose synthase enzyme activity, distribution of cell wall polysaccharide, tube nuclei movement. Treatment of 0.01 mM spermidine which showed a positive effect, increased actin dynamism, and, caused a decrease in the amount of cellulose in the tube apex by coordinating the sucrose synthase enzyme localization. These changes were reflected in the tube elongation velocities and oscillations as an increase, allowing the tubes to elongate faster. Treatment of 0.5 mM spermidine which showed a negative effect, caused changes in intracellular calcium, pH and reactive oxygen species gradients and these alterations reduced the dynamism of actin filaments. Decreased actin dynamism affected the localization of the sucrose synthase enzyme, inhibited the transport of newly synthesized wall materials to the tube apex and the transport of the generative nucleus to the tube apex. These changes were reflected in the tube elongation velocities and oscillations as a decrease, allowing the tubes to elongate slower. Results could be contributed to the explanation of the effect of spermidine in plant growth and development, including pollen tube elongation.
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References
Abbasi NA, Ali I, Hafiz IA, Khan AS (2017) Application of polyamines in horticulture: a review. Int J Biosci 10(5):319–342. https://doi.org/10.12692/ijb/10.5.319-342
Aloisi I, Cai G, Tumiatti V, Minarini A, Del Duca S (2015) Natural polyamines and synthetic analogs modify the growth and the morphology of Pyrus communis pollen tubes affecting ROS levels and causing cell death. Plant Sci 239:92–105. https://doi.org/10.1016/j.plantsci.2015.07.008
Aloisi I, Cai G, Serafini-Fracassini D, Del Duca S (2016) Polyamines in pollen: from microsporogenesis to fertilization. Front Plant Sci 7:155. https://doi.org/10.3389/fpls.2016.00155
Aloisi I, Cai G, Faleri C, Navazio L, Serafini-Fracassini D, Del Duca S (2017) Spermine regulates pollen tube growth by modulating Ca2+-dependent actin organization and cell wall structure. Front Plant Sci 8:1701. https://doi.org/10.3389/fpls.2017.01701
Aloisi I, Piccini C, Cai G, Del Duca S (2022) Male fertility under environmental stress: Do polyamines act as pollen tube growth protectants? Int J Mol Sci 23(3):1874. https://doi.org/10.3390/ijms23031874
Benko P, Jee S, Kaszler N, Fehér A, Gémes 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
Boudaoud A, Burian A, Borowska-Wykręt D, Uyttewaal M, Wrzalik R, Kwiatkowska D, Hamant O (2014) FibrilTool, an ImageJ plug-in to quantify fibrillar structures in raw microscopy images. Nat Protoc 9:457–463. https://doi.org/10.1038/nprot.2014.024
Brewbaker JL, Kwack BH (1963) The essential role of calcium ion pollen germination and pollen tube growth. Am J Bot 50(9):859–865. https://doi.org/10.1002/j.1537-2197.1963.tb06564.x
Cai G (2022) The legacy of kinesins in the pollen tube 30 years later. Cytoskeleton 79(1–3):8–19. https://doi.org/10.1002/cm.21713
Cai G, Parrotta L, Cresti M (2015) Organelle trafficking, the cytoskeleton, and pollen tube growth. J Integr Plant Biol 57:63–78. https://doi.org/10.1111/jipb.12289
Calic D, Devrnja N, Kostic I, Kostic M (2013) Pollen morphology, viability, and germination of Prunus domestica cv. Požegača Sci Hortic 155:118–122. https://doi.org/10.1016/j.scienta.2013.03.017
Cardenas L, Lovy-Wheeler A, Wilsen KL, Hepler PK (2005) Actin polymerization promotes the reversal of streaming in the apex of pollen tubes. Cell Motil Cytoskelet 61(2):112–127. https://doi.org/10.1002/cm.20068
Çetinbaş-Genç A, Cai G, Del Duca S (2020a) Treatment with spermidine alleviates the effects of concomitantly applied cold stress by modulating Ca2+, pH and ROS homeostasis, actin filament organization and cell wall deposition in pollen tubes of Camellia sinensis. Plant Physiol Biochem 156:578–590. https://doi.org/10.1016/j.plaphy.2020.10.008
Çetinbaş-Genç A, Cai G, Del Duca S, Vardar F, Ünal M (2020b) The effect of putrescine on pollen performance in hazelnut (Corylus avellana L.). Sci Hortic 261:108971. https://doi.org/10.1016/j.scienta.2019.108971
Çetinbaş-Genç A, Conti V, Cai G (2022) Let’s shape again: the concerted molecular action that builds the pollen tube. Plant Reprod 35:77–103. https://doi.org/10.1007/s00497-022-00437-4
Charnay D, Nari J, Norat G (1992) Regulation of plant cell-wall pectin methyl esterase by polyamines-interactions with the effects of metal ions. Eur J Biochem 205(2):711–714. https://doi.org/10.1111/j.1432-1033.1992.tb16833.x
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(2):703–715. https://doi.org/10.1104/pp.110.155457
Dai Q, Peng S, Chavez AQ, Vergara BS (1994) Intraspecific response of 188 rice cultivars to enhanced UVB radiation. Environ Exp Bot 34(4):433–442. https://doi.org/10.1016/0098-8472(94)90026-4
Del Duca S, Bregoli AM, Bergamini C, Serafini-Fracassini D (1997) Transglutaminase-catalyzed modification of cytoskeletal proteins by polyamines during the germination of Malus domestica pollen. Sex Plant Reprod 10:89–95. https://doi.org/10.1007/s004970050072
Del Duca S, Serafini-Fracassini D, Bonner P, Cresti M, Cai G (2009) Effects of post-translational modifications catalysed by pollen transglutaminase on the functional properties of microtubules and actin filaments. Biochem J 418(3):651–664. https://doi.org/10.1042/BJ20081781
Del Duca S, Faleri C, Iorio RA, Cresti M, Serafini-Fracassini D, Cai G (2013) Distribution of transglutaminase in pear pollen tubes in relation to cytoskeleton and membrane dynamics. Plant Physiol 161(4):1706–1721. https://doi.org/10.1104/pp.112.212225
Derksen J, Knuiman B, Hoedemaekers K, Guyon A, Bonhomme S, Pierson ES (2002) Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sex Plant Reprod 15:133–139. https://doi.org/10.1007/s00497-002-0149-1
Desnoyer NJ, Grossniklaus U (2023) Live imaging of Arabidopsis pollen tube reception and double fertilization using the semi-in vitro cum septum method. J vis Exp 192:e65156. https://doi.org/10.3791/65156
Di Sandro A, Del Duca S, Verderio E, Hargreaves AJ, Scarpellini A, Cai G, Cresti M, Faleri C, Iorio RA, Hirose S, Furutani Y, Coutts IGC, Griffin M, Bonner PLR, Serafini-Fracassini D (2010) An extracellular transglutaminase is required for apple pollen tube growth. Biochem J 429(2):261–271. https://doi.org/10.1042/BJ20100291
Do THT, Choi H, Palmgren M, Martinoia E, Hwang JU, Lee Y (2019) Arabidopsis ABCG28 is required for the apical accumulation of reactive oxygen species in growing pollen tubes. Proc Natl Acad Sci 116(25):12540–12549. https://doi.org/10.1073/pnas.1902010116
Dong H, Pei W, Haiyun R (2012) Actin fringe is correlated with tip growth velocity of pollen tubes. Mol Plant 5:1160–1162. https://doi.org/10.1093/mp/sss073
Feijó JA, Sainhas J, Hackett GR, Kunkel JG, Hepler PK (1999) Growing pollen tubes possess a constitutive alkaline band in the clear zone and a growth-dependent acidic tip. J Cell Biol 144(3):483–496. https://doi.org/10.1083/jcb.144.3.483
Fricker MD, White NS, Obermeyer G (1997) pH gradients are not associated with tip growth in pollen tubes of Lilium longiflorum. J Cell Sci 110(15):1729–1740. https://doi.org/10.1242/jcs.110.15.1729
Geitmann A, Li YQ, Cresti M (1996) The role of the cytoskeleton and dictyosome activity in the pulsatory growth of Nicotiana tabacum and Petunia hybrida pollen tubes. Plant Biol 109(2):102–109. https://doi.org/10.1111/j.1438-8677.1996.tb00549.x
Hepler PK (2016) The cytoskeleton and its regulation by calcium and protons. Plant Physiol 170(1):3–22. https://doi.org/10.1104/pp.15.01506
Hepler PK, Rounds CM, Winship LJ (2013) Control of cell wall extensibility during pollen tube growth. Mol Plant 6(4):998–1017. https://doi.org/10.1093/mp/sst103
Hoffmann RD, Portes MT, Olsen LI, Damineli DSC, Hayashi M, Nunes CO, Pedersen JT, Lima PT, Campos C, Feijo JA, Palmgren M (2020) Plasma membrane H+-ATPases sustain pollen tube growth and fertilization. Nat Commun 11:2395. https://doi.org/10.1038/s41467-020-16253-1
Kapoor K, Geitmann A (2023) Pollen tube invasive growth is promoted by callose. Plant Reprod. https://doi.org/10.1007/s00497-023-00458-7
Kaya H, Nakajima R, Iwano M, Kanaoka MM, Kimura S, Takeda S, Kawarazak 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(3):1069–1080. https://doi.org/10.1105/tpc.113.120642
Kolupaev YE, Kokorev AI, Dmitriev AP (2022) Polyamines: involvement in cellular signaling and plant adaptation to the effect of abiotic stressors. Cytol Genet 56(2):148–163. https://doi.org/10.3103/S0095452722020062
Konrad KR, Wudick MM, Feijo JA (2011) Calcium regulation of tip growth: new genes for old mechanisms. Curr Opin Plant Biol 14(6):721–730. https://doi.org/10.1016/j.pbi.2011.09.005
Koti S, Reddy KR, Kakani VG, Zhao D, Reddy VR (2004) Soybean (Glycine max) pollen germination characteristics, flower and pollen morphology in response to enhanced ultraviolet-B radiation. Ann Bot 94(6):855–864. https://doi.org/10.1093/aob/mch212
Koubouris GC, Metzidakis IT, Vasilakakis MD (2009) Impact of temperature on olive (Olea europaea L.) pollen performance in relation to relative humidity and genotype. Environ Exp Bot 67(1):209–214. https://doi.org/10.1016/j.envexpbot.2009.06.002
Kroeger JH, Geitmann A, Grant M (2008) Model for calcium dependent oscillatory growth in pollen tubes. J Theor Biol 253(2):363–374. https://doi.org/10.1016/j.jtbi.2008.02.042
Laitiainen E, Nieminen KM, Vihinen H, Raudaskoski M (2002) Movement of generative cell and vegetative nucleus in tobacco pollen tubes is dependent on microtubule cytoskeleton but independent of synthesis of callose plugs. Sex Plant Reprod 15:195–204. https://doi.org/10.1007/s00497-002-0155-3
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. https://doi.org/10.1111/tpj.12452
Liu X, Xiao Y, Zi J, Yan J, Li C, Du C, Wan J, Wu H, Zheng B, Wang S, Liang Q (2023) Differential effects of low and high temperature stress on pollen germination and tube length of mango (Mangifera indica L.) genotypes. Sci Rep 13(1):1–14. https://doi.org/10.1038/s41598-023-27917-5
Lovy-Wheeler A, Wilsen KL, Baskin TI, Hepler PK (2005) Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube. Planta 221:95–104. https://doi.org/10.1007/s00425-004-1423-2
Lu Q, Liu X, Qu X, Huang S (2023) Visualization and quantification of the dynamics of actin filaments in Arabidopsis pollen tubes. In: Hussey PJ, Wang P (eds) The plant cytoskeleton. Methods in molecular biology. Humana, New York, pp 285–295
Monteiro D, Liu Q, Lisboa S, Scherer GEF, Quader H, Malho R (2005) Phosphoinositides and phosphatidic acid regulate pollen tube growth and reorietation through modulation of (Ca2+)C and membrane secretion. J Exp Bot 56(416):1665–1674. https://doi.org/10.1093/jxb/eri163
Parrotta L, Faleri C, Cresti M, Cai G (2016) Heat stress affects the cytoskeleton and the delivery of sucrose synthase in tobacco pollen tubes. Planta 243:43–63. https://doi.org/10.1007/s00425-015-2394-1
Parrotta L, Faleri C, Del Duca S, Cai G (2018) Depletion of sucrose induces changes in the tip growth mechanism of tobacco pollen tubes. Ann Bot 122(1):23–43. https://doi.org/10.1093/aob/mcy043
Parrotta L, Faleri C, Guerriero G, Cai G (2019) Cold stress affects cell wall deposition and growth pattern in tobacco pollen tubes. Plant Sci 283:329–342. https://doi.org/10.1016/j.plantsci.2019.03.010
Parrotta L, Faleri C, Del Casino C, Mareri L, Aloisi I, Guerriero G, Hausman JF, Del Duca S, Cai G (2022) Biochemical and cytological interactions between callose synthase and microtubules in the tobacco pollen tube. Plant Cell Rep 41:1301–1318. https://doi.org/10.1007/s00299-022-02860-3
Persia D, Cai G, Del Casino C, Faleri C, Willemse MT, Cresti M (2008) Sucrose synthase is associated with the cell wall of tobacco pollen tubes. Plant Physiol 147:1603–1618. https://doi.org/10.1104/pp.108.115956
Polito VS (1983) Membrane-associated calcium during pollen grain germination: a microfluorometric analysis. Protoplasma 117:226–232. https://doi.org/10.1007/BF01281826
Potocky M, Pejchar P, Gutkowska M, Jimenez-Quesada MJ, Potocka A, de Dios AJ, Kost B, Zarsk V (2012) NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. J Plant Physiol 169(16):1654–1663. https://doi.org/10.1016/j.jplph.2012.05.014
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154. https://doi.org/10.3389/fpls.2014.00154
Poulter NS, Vatovec S, Franklin-Tong VE (2008) Microtubules are a target for self-incompatibility signaling in Papaver pollen. Plant Physiol 146(3):1358–1367. https://doi.org/10.1104/pp.107.107052
Qian D, Xiang Y (2019) Actin cytoskeleton as actor in upstream and downstream of calcium signaling in plant cells. Int J Mol Sci 20(6):1403. https://doi.org/10.3390/ijms20061403
Rounds CM, Lubeck E, Hepler PK, Winship LJ (2011) Propidium iodide competes with Ca2+ to label pectin in pollen tubes and Arabidopsis root hairs. Plant Physiol 157(1):175–187. https://doi.org/10.1104/pp.111.182196
Scholz P, Anstatt J, Krawczyk HE, Ischebeck T (2020) Signaling pinpointed to the tip: the complex regulatory network that allows pollen tube growth. Plants 9(9):1098. https://doi.org/10.3390/plants9091098
Song J, Nada K, Tachibana S (1999) Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersicum esculentum Mill.). Sci Hortic 80(3–4):203–212. https://doi.org/10.1016/S0304-4238(98)00254-4
Sorkheh K, Azimkhani R, Mehri N, Chaleshtori MH, Halasz J, Ercisli S, Koubouris GC (2018) Interactive effects of temperature and genotype on almond (Prunus dulcis L.) pollen germination and tube length. Sci Hortic 227:162–168. https://doi.org/10.1016/j.scienta.2017.09.037
Sorkheh K, Shiran B, Rouhi V, Khodambashi M, Wolukau JN, Ercisli S (2011) Response of in vitro pollen germination and pollen tube growth of almond (Prunus dulcis Mill.) to temperature, polyamines and polyamine synthesis inhibitor. Biochem Syst Ecol 39(4-6):749–757. https://doi.org/10.1016/j.bse.2011.06.015
Steinhorst L, Kudla J (2013) Calcium: a central regulator of pollen germination and tube growth. Biochim Biophys Acta BBA Mol Cell Res 1833:1573–1581. https://doi.org/10.1016/j.bbamcr.2012.10.009
Wang Q, Lu L, Wu X, Li Y, Lin J (2003) Boron influences pollen germination and pollen tube growth in Picea meyeri. Tree Physiol 23:345–351. https://doi.org/10.1093/treephys/23.5.345
Winship L, Rounds C, Hepler P (2017) Perturbation analysis of calcium, alkalinity and secretion during growth of Lily pollen tubes. Plants 6:3. https://doi.org/10.3390/plants6010003
Wolukau JN, Zhang S, Xu G, Chen D (2004) The effect of temperature, polyamines and polyamine synthesis inhibitor on in vitro pollen germination and pollen tube growth of Prunus mume. Sci Hortic 99(3–4):289–299. https://doi.org/10.1016/S0304-4238(03)00112-2
Wu J, Shang Z, Wu J, Jiang X, Moschou PN, Sun W, Roubelakis-Angelakis KA, Zhang S (2010) Spermidine oxidase-derived H2O2 regulates pollen plasma membrane hyperpolarization-activated Ca2+-permeable channels and pollen tube growth. Plant J 63(6):1042–1053. https://doi.org/10.1111/j.1365-313X.2010.04301.x
Zhang R, Xu Y, Yi R, Shen J, Huang S (2023) Actin cytoskeleton in the control of vesicle transport, cytoplasmic organization and pollen tube tip growth. Plant Physiol 00:1–17. https://doi.org/10.1093/plphys/kiad203
Acknowledgements
Çiğdem Tunur would like to acknowledge The Scientific And Technological Research Council Of Türkiye (TÜBİTAK) for providing scholarship with 2210-A National Graduate Scholarship Program. This work was financially supported by the Marmara University Scientific Research Projects Commission (Project no: FYL-2022-10575).
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Tunur, Ç., Çetinbaş-Genç, A. Spermidine Modulates Pollen Tube Growth by Affecting the Factors Involved in Pollen Tube Elongation. J Plant Growth Regul 43, 1166–1183 (2024). https://doi.org/10.1007/s00344-023-11174-x
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DOI: https://doi.org/10.1007/s00344-023-11174-x