Pollen performance of pomegranate under high-temperature stress

Abstract

The high-temperature stress (30 °C, 35 °C, 40 °C) response of pollen performance in Punica granatum was analyzed. Pollen germination rate and tube length were significantly inhibited after 35 °C and 40 °C treatment. According to cumulative stress response index values, 40 °C had the most destructive impact. High-temperature stress caused various abnormalities at tubes, especially at apex and the most common abnormalities were marked change of elongation direction and swelling. Although dense callose accumulation and increase in apex-localized reactive oxygen species was noticed at the apex after 35 °C and 40 °C temperature treatment, the most harmful temperature was stated as 40 °C.

Keywords

• High-temperature
• pollen germination
• pollen tube
• Punica granatum

Yüksek sıcaklık stresi altında narın polen performansı

Abstract

Bu çalışmada Punica granatum'da polen performansının yüksek sıcaklık stresine (30 °C, 35 °C, 40 °C) olan tepkisi analiz edildi. Polen çimlenme oranı ve tüp uzunluğu 35 °C ve 40 °C uygulamasından sonra istatistiksel olarak anlamlı bir şekilde azaldı. Kümülatif stres tepki indeksi değerlerine göre, 40 °C polen performansı üzerinde en yıkıcı etkiye sahipti. Yüksek sıcaklık stresi polen tüplerinin özellikle uçlarında çeşitli anormalliklere neden oldu. En yaygın görülen anormallikler uzama yönünün değişmesi ve tüp uçlarının şişmesiydi. 35 °C ve 40 °C uygulamalarından sonra tüp uçlarında yoğun kalloz birikimi ve reaktif oksijen türlerinde artış görülmesine rağmen, en yıkıcı yüksek sıcaklık stresi 40 °C olarak belirlendi.

Keywords

• polen çimlenmesi
• polen tüpü
• Punica granatum
• yüksek sıcaklık

References

1. 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.
2. Boavida LC, McCormick S (2007). Technical advance: Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. The Plant Journal 52(3): 570-582.
3. Boussaa F, Zaouay F, Burlo-Carbonell F, Noguera-Artiaga L, Carbonell-Barrachina A, Melgarejo P, Hernandez F, Mars M (2020). Growing location affects physical properties, bioactive compounds, and antioxidant activity of pomegranate fruit (Punica granatum L. var. gabsi). International Journal of Fruit Science 20: 508-523.
4. Brewbaker JL, Kwack BH (1963). The essential role of calcium ion in pollen germination and pollen tube growth. American Journal of Botany 50(9): 859-865.
5. Cai G, Faleri C, Del Casino C, Emons AMC, Cresti M (2011). Distribution of callose synthase, cellulose synthase, and sucrose synthase in tobacco pollen tube is controlled in dissimilar ways by actin filaments and microtubules. Plant Physiol 155(3): 1169-1190.
6. Cascallares M, Setzes N, Marchetti F, López GA, Distéfano AM, Cainzos M, Zabaleta E, Pagnussat GC (2020). A Complex journey: cell wall remodeling, ınteractions, and ıntegrity during pollen tube growth. Frontiers in Plant Science 11: 599247.
7. Chen T, Teng N, Wu X, Wang Y, Tang W, Samaj J, Baluska F, Lin J (2007). Disruption of actin filaments by latrunculin B affects cell wall construction in Picea meyeri pollen tube by disturbing vesicle trafficking. Plant Cell Physiology 48: 19-30.
8. Çetinbaş-Genç A, Ünal M (2017) Timing of reproductive organs maturity in proterandrous Malva sylvestris L. Notulae Scientia Biologicae 9(2): 287-295.

9. Çetinbaş-Genç A, Cai G, Vardar F, Ünal M (2019). Differential effects of low and high temperature stress on pollen germination and tube length of hazelnut (Corylus avellana L.) genotypes. Scientia Horticulturae 255: 61-69.
10. Dai Q, Shaobing P, Chavez AQ, Vergara BS (1994). Intraspecific responses of 188 rice cultivars to enhanced UVB radiation. Environmental and Experimental Botany 34(4): 433-442.
11. Engin H, Gökbayrak Z (2016). In vitro pollen viability and germination of bisexual and functional male flowers of some Turkish pomegranate cultivars. Agriculture & Forestry 62(4): 91-94.
12. Engin H, Hepaksoy S (2003). Bazı nar çeşitlerinin çiçek tozu çimlenme güçlerinin belirlenmesi. Ege Üniversitesi Ziraat Fakültesi Dergisi 40(3): 9-16.
13. Ferguson JN, Tidy AC, Murchie EH, Wilson ZA (2021). The potential of resilient carbon dynamics for stabilizing crop reproductive development and productivity during heat stress. Plant, Cell & Environment 44(7): 2066-2089.
14. Gadže J, Radunic M, Petric IV, Ercisli S (2011). In vitro pollen viability, germination and pollen tube growth in some pomegranate (Punica granatum L.) cultivars from Croatia and Bosnia and Herzegovina. Acta Scientiarum Polonorum Hortorum Cultus 10: 297-305.
15. Gökbayrak Z, Engin H (2018). Effects of foliar-applied brassinosteroid on viability and ın vitro germination of pollen collected from bisexual and functional male flowers of pomegranate. International Journal of Fruit Science 18(2): 226-230.
16. Hao H, Chen T, Fan L, Li R, Wang X (2013). 2, 6-dichlorobenzonitrile causes multiple effects on pollen tube growth beyond altering cellulose synthesis in Pinus bungeana Zucc. PLoS One, 8(10): e76660.
17. Kakani VG, Prasad PV, Craufurd PQ, Wheeler TR (2002). Response of in vitro pollen germination and pollen tube growth of groundnut (Arachis hypogaea L.) genotypes to temperature. Plant Cell and Environmental 25(12): 1651-1661.
18. Kapoor K, Geitmann A (2023). Pollen tube invasive growth is promoted by callose. Plant Reproduction 36717422 (in print).
19. Khemakhem M, Zarroug Y, Jabou K, Selmi S, Bouzouita N (2021). Physicochemical characterization of oil, antioxidant potential, and phenolic profile of seeds isolated from Tunisian pomegranate (Punica granatum L.) cultivars. Journal of Food Science 86(3): 852-859.
20. Korkmaz N, Güneri M (2019). Effect of different boron levels on pollen germination of Hicaz nar pomegranate (Punica granatum L.) cultivar. International Journal of Agriculture Forestry and Life Sciences 3(1): 151-156.
21. Koubouris GC, Metzidakis IT, Vasilakakis MD (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.
22. Krawczyk HE, Rotsch AH, Herrfurth C, Scholz P, Shomroni O, Salinas-Riester G, Feussner I, Ischebeck T (2022). Heat stress leads to rapid lipid remodeling and transcriptional adaptations in Nicotiana tabacum pollen tubes. Plant Physiology 189(2): 490-515.
23. Mesihovic A, Iannacone R, Firon N, Fragkostefanakis S (2016). Heat stress regimes for the investigation of pollen thermotolerance in crop plants. Plant Reproduction 29: 93-105.
24. Moga MA, Dimienescu OG, Bălan A, Dima L, Toma SI, Bîgiu NF, Blidaru A (2021). Pharmacological and therapeutic properties of Punica granatum phytochemicals: Possible roles in breast cancer. Molecules 26(4): 1054.
25. Morbey YE, Ydenberg RC (2001). Protandrous arrival timing to breeding areas: a review. Ecology Letters 4(6): 663-673.
26. Muhlemann JK, Younts TL, Muday GK (2018) Flavonols control pollen tube growth and integrity by regulating ROS homeostasis during high-temperature stress. PNAS 115(47): E11188–E11197.
27. Parrotta L, Faleri C, Guerriero G, Cai G (2019). Cold stress afects cell wall deposition and growth pattern in tobacco pollen tubes. Plant Sciences 283: 329-342.
28. 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.
29. 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 Reports 41(5): 1301-1318.
30. Qin P, Ting D, Shieh A, McCormick S (2012). Callose plug deposition patterns vary in pollen tubes of Arabidopsis thaliana ecotypes and tomato species. BMC Plant Biology 12: 178.
31. Scholz P, Anstatt J, Krawczyk HE, Ischebeck T (2020). Signalling pinpointed to the tip: the complex regulatory network that allows pollen tube growth. Plants 9(9): 1098.
32. Song G, Wang M, Zeng B, Zhang J, Jiang C, Hu Q, Geng G, Tang C (2015) Anther response to high-temperature stress during development and pollen thermotolerance heterosis as revealed by pollen tube growth and in vitro pollen vigor analysis in upland cotton. Planta 241: 1271-1285.
33. 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. Scientia Horticulturae 227: 162-168.
34. Srinivasan A, Saxena N, Johansen C (1999). Cold tolerance during early reproductive growth of chickpea (Cicer arietinum L.): genetic variation in gamete development and function. Field Crops Research 60: 209-222.
35. Swanson S, Gilroy S (2010). ROS in plant development. Physiologia Plantarum 138(4): 384-392.
36. Teniente SL, Flores-Gallegos AC, Esparza-González SC, Campos-Múzquiz LG, Nery-Flores SD, Rodríguez-Herrera R (2023). Anticancer effect of pomegranate peel polyphenols against cervical cancer. Antioxidants 12(1): 127.
37. Wang W, Sheng X, Shu Z, Li D, Pan J, Ye X, Chang P, Li X, Wang Y (2016). Combined cytological and transcriptomic analysis reveals a nitric oxide signaling pathway involved in cold-inhibited Camellia sinensis pollen tube growth. Frontiers in Plant Science 7: 456.
38. 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.
39. Wetzstein HY, Ravid N, Wilkins E, Martinelli AP (2011). A morphological and histological characterization of bisexual and male flower types in pomegranate. Journal of the American Society for Horticultural Science 136(2): 83-92.
40. You J, Chan Z (2015). ROS regulation during abiotic stress responses in crop plants. Frontiers in Plant Science 6: 1092.
41. Zhu T, Fonseca De Lima CF, De Smet I (2021). The heat is on: how crop growth, development, and yield respond to high temperature. Journal of Experimental Botany 72(21): 37359-7373.
42. Zonia L (2010). Spatial and temporal integration of signalling networks regulating pollen tube growth. Journal of Experimental Botany 61: 1939-1957.