The Responses of Pollen Tubes to Spermidine Treatments in Actinidia deliciosa

Abstract

In this study, the responses of pollen tubes to spermidine treatments (10 µM, 25 µM, 50 µM, 100 µM, 250 µM, or 500 µM) were investigated in Actinidia deliciosa, by focusing on pollen germination rate, pollen tube length, organizations of actin filaments, concentrations of Ca+2, pH, reactive oxygen species and distributions of callose and cellulose. According to findings, the only positive effect was detected after 10 µM spermidine treatment while the most negative acute effect was detected after 500 µM spermidine treatment and, further experiments were done in these groups. 10 µM spermidine increased the pollen tube length by changing the concentration of apex localized reactive oxygen species. 500 µM spermidine decreased the pollen tube length by changing the apex localized Ca+2, pH, and reactive oxygen species concentration. Findings would contribute to the understanding of the effects of polyamines on pollen tubes.

Keywords

• Actin cytoskeleton
• cell wall
• pollen tube
• polyamine
• spermidine

Actinidia deliciosa’da Polen Tüplerinin Spermidin Uygulamalarına Verdiği Yanıtlar

Öz

Bu çalışmada Actinidia deliciosa'da polen tüplerinin spermidin uygulamalarına (10 µM, 25 µM, 50 µM, 100 µM, 250 µM veya 500 µM) verdiği yanıtlar, polen çimlenme oranı, polen tüp uzunluğu, aktin filament organizasyonu, Ca+2, pH, reaktif oksijen türlerinin konsantrasyonu ve kalloz ve selüloz dağılımına odaklanarak incelenmiştir. Bulgulara göre tek olumlu etki 10 µM spermidine uygulamasından sonra tespit edilirken, en olumsuz akut etki 500 µM spermidine uygulamasından sonra tespit edilmiş ve ileri deneyler bu gruplarda yapılmıştır. 10 µM spermidin, apekste lokalize olan reaktif oksijen türlerinin konsantrasyonunu değiştirerek polen tüpü uzunluğunu arttırmıştır. 500 µM spermidin ise apekste lokalize olan Ca+2, pH ve reaktif oksijen türlerinin konsantrasyonunu değiştirerek polen tüpü uzunluğunu azaltmıştır. Bulguların poliaminlerin polen tüpleri üzerindeki etkilerinin anlaşılmasına katkıda bulunabileceği düşünülmektedir.

Anahtar Kelimeler

• aktin hücre iskeleti
• hücre çeperi
• polen tüpü
• poliamin
• spermidin

Kaynakça

1. Aloisi, I., Cai, G., Serafini-Fracassini, D., & Del Duca, S. (2016). Polyamines in pollen: from microsporogenesis to fertilization. Frontiers in Plant Science, 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. Frontiers in Plant Science, 8, 1701. https://doi.org/10.3389/fpls.2017.01701
2. Aloisi, I., Piccini, C., Cai, G., & Del Duca, S. (2022). Male fertility under environmental stress: Do polyamines act as pollen tube growth protectants?. International Journal of Molecular Sciences, 23(3), 1874. https://doi.org/10.3390/ijms23031874
3. 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. Journal Of Plant Physiology, 244, 153085. https://doi.org/10.1016/j.jplph.2019.153085
4. 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. Nature Protocols, 9(2), 457-463. https://doi.org/10.1038/nprot.2014.024
5. Cai, G., Parrotta, L., & Cresti, M. (2015). Organelle trafficking, the cytoskeleton, and pollen tube growth. Journal of Integrative Plant Biology, 57(1), 63-78. https://doi.org/10.1111/jipb.12289
6. Çetinbaş-Genç, A., Cai, G., & Del Duca, S. (2020). 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 Physiology and Biochemistry, 156, 578-590. https://doi.org/10.1016/j.plaphy.2020.10.008
7. Dai, Q., Shaobing, P., Chavez, A. Q., & Vergara, B. S. (1994). Intraspecific responses of 188 rice cultivars to enhanced UVB radiation. Environmental and Experimental Botany, 34(4), 433-442. https://doi.org/10.1016/0098-8472(94)90026-4
8. Del Duca, S., Bregoli, A. M., Bergamini, C., & Serafini-Fracassini, D. (1997). Transglutaminase-catalyzed modification of cytoskeletal proteins by polyamines during the germination of Malus domestica pollen. Sexual Plant Reproduction, 10, 89-95. https://doi.org/10.1007/s004970050072

9. Del Duca, S., Faleri, C., Iorio, R. A., Cresti, M., Serafini-Fracassini, D., & Cai, G. (2013). Distribution of transglutaminase in pear pollen tubes in relation to cytoskeleton and membrane dynamics. Plant Physiology, 161(4), 1706-1721. https://doi.org/10.1104/pp.112.212225
10. Derksen, J., Knuiman, B., Hoedemaekers, K., Guyon, A., Bonhomme, S., & Pierson, E. S. (2002). Growth and cellular organization of Arabidopsis pollen tubes in vitro. Sexual Plant Reproduction, 15, 133-139. https://doi.org/10.1007/s00497-002-0149-1
11. Dutta, S. K., Layek, J., Yadav, A., Das, S. K., Rymbai, H., Mandal, S., Shana, S., Bhutia, T.L., Devi, E. L., Patel, V. B., Laha, R., & Mishra, V. K. (2023). Improvement of rooting and growth in kiwifruit (Actinidia deliciosa) cuttings with organic biostimulants. Heliyon, 9(7). https://doi.org/10.1016/j.heliyon.2023.e17815
12. Garg, A. K., Kaushal, R., Rana, V. S., & Singh, P. (2023). Assessment of yield, quality and economics of kiwifruit (Actinidia deliciosa cv. Allison) production as influenced by integrated nitrogen management strategies in Indian Lower Himalayas. Journal of Soil Science and Plant Nutrition, 1-19. https://doi.org/10.1007/s42729-023-01429-7
13. Güçlü, S. F., Öncü, Z., & Koyuncu, F. (2020). Pollen performance modelling with an artificial neural network on commercial stone fruit cultivars. Horticulture, Environment, and Biotechnology, 61(1), 61-67. https://doi.org/10.1007/s13580-019-00208-7
14. Jinming, X. U., Yihong, C. H. A. N. G., Han, G. O. N. G., Wenfang, G. O. N. G., & Deyi, Y. U. A. N. (2023). Effects of different exogenous substances on pollen germination and pollen tube growth of Camellia oleifera. Acta Agriculturae Zhejiangensis, 35(4), 789.
15. Kapoor, K., & Geitmann, A. (2023). Pollen tube invasive growth is promoted by callose. Plant Reproduction, 1-15. https://doi.org/10.1007/s00497-023-00458-7
16. Koubouris, G. C., Metzidakis, I. T., & Vasilakakis, M. D. (2009). Impact of temperature on olive (Olea europaea L.) pollen performance in relation to relative humidity and genotype. Environmental and Experimental Botany, 67(1), 209-214. https://doi.org/10.1016/j.envexpbot.2009.06.002
17. Lovy-Wheeler, A., Wilsen, K. L., Baskin, T. I., & Hepler, P. K. (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
18. Malho, R., Camacho, L., & Moutinho, A. (2000). Signalling pathways in pollen tube growth and reorientation. Annals of Botany, 85, 59-68. https://doi.org/10.1006/anbo.1999.0991
19. Nie, S., Zheng, S., Lyu, C., Cui, S., Huo, J., & Zhang, L. (2023). Calcium/calmodulin modulates pollen germination and pollen tube growth and self-incompatibility response in Chinese cabbage (Brassica rapa L.). Scientia Horticulturae, 308, 111607. https://doi.org/10.1016/j.scienta.2022.111607
20. Parrotta, L., Faleri, C., Del Casino, C., Mareri, L., Aloisi, I., Guerriero, G., Hausman, J. F., Del Duca, S., & Cai, G. (2022). Biochemical and cytological interactions between callose synthase and microtubules in the tobacco pollen tube. Plant Cell Reports, 41(5), 1301-1318. https://doi.org/10.1007/s00299-022-02860-3
21. Potocky, M., Pejchar, P., Gutkowska, M., Jiménez-Quesada, M. J., Potocká, A., de Dios Alché, J., Kost, B., & Žárský, V. (2012). NADPH oxidase activity in pollen tubes is affected by calcium ions, signaling phospholipids and Rac/Rop GTPases. Journal of Plant Physiology, 169(16), 1654-1663. https://doi.org/10.1016/j.jplph.2012.05.014
22. Serrazina, S., Dias, F. V., & Malhó, R. (2014). Characterization of FAB 1 phosphatidylinositol kinases in Arabidopsis pollen tube growth and fertilization. New Phytologist, 203(3), 784-793. https://doi.org/10.1111/nph.12836
23. Song, J., Nada, K., & Tachibana, S. (1999). Ameliorative effect of polyamines on the high temperature inhibition of in vitro pollen germination in tomato (Lycopersicon esculentum Mill.). Scientia Horticulturae, 80(3-4), 203-212. https://doi.org/10.1016/S0304-4238(98)00254-4
24. Sorkheh, K., Shiran, B., Rouhi, V., Khodambashi, M., Wolukau, J. N., & 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. Biochemical Systematics and Ecology, 39(4-6), 749-757. https://doi.org/10.1016/j.bse.2011.06.015
25. Sorkheh, K., Azimkhani, R., Mehri, N., Chaleshtori, M. H., Halász, J., Ercisli, S., & Koubouris, G. C. (2018). Interactive effects of temperature and genotype on almond (Prunus dulcis L.) pollen germination and tube length. Scientia horticulturae, 227, 162-168. https://doi.org/10.1016/j.scienta.2017.09.037
26. Tang, C., Wang, P., Zhu, X., Qi, K., Xie, Z., Zhang, H., Li, X., Gao, H., Gu, T., Gu, C., Li, S., De Graff, B. H. J, Zhang, S, & Wu, J. (2023). Acetylation of inorganic pyrophosphatase by S-RNase signaling induces pollen tube tip swelling by repressing pectin methylesterase. The Plant Cell, 162. https://doi.org/10.1093/plcell/koad162
27. Vogler, F., Schmalzl, C., Englhart, M., Bircheneder, M., & Sprunck, S. (2014). Brassinosteroids promote Arabidopsis pollen germination and growth. Plant Reproduction, 27, 153-167. https://doi.org/10.1007/s00497-014-0247-x
28. Wang, Q., Lu, L., Wu, X., Li, Y., & Lin, J. (2003). Boron influences pollen germination and pollen tube growth in Picea meyeri. Tree physiology, 23(5), 345-351.https://doi.org/10.1093/treephys/23.5.345
29. Wolukau, J. N., 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. Scientia Horticulturae, 99(3-4), 289-299. https://doi.org/10.1016/S0304-4238(03)00112-2
30. Wu, J., Shang, Z., Wu, J., Jiang, X., Moschou, P. N., Sun, W., Roubelakis-Angelakis, K. A., & Zhang, S. (2010). Spermidine oxidase‐derived H2O2 regulates pollen plasma membrane hyperpolarization‐activated Ca2+‐permeable channels and pollen tube growth. The Plant Journal, 63(6), 1042-1053. https://doi.org/10.1111/j.1365-313X.2010.04301.x
31. 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 Physiology, 203. https://doi.org/10.1093/plphys/kiad203
32. Zhao, W., Hou, Q., Qi, Y., Wu, S., & Wan, X. (2023). Structural and molecular basis of pollen germination. Plant Physiology and Biochemistry, 108042. https://doi.org/10.1016/j.plaphy.2023.108042