В огляді розглядаються історичні аспекти відкриття стриголактонів, формування й розширення уявлень про їхню фізіологічну роль, класифікація природних стриголактонів та їх ізомерів, видоспецифічність, головні структурні особливості, участь в адаптації рослин до дії стресових чинників і взаємодія з іншими фітогормонами. Відзначено, що стриголактони мають специфічний вплив на різні види рослин-паразитів. Різноманітність фізіологічних функцій стриголактонів наведена для багатьох систем рослинних організмів. Доведено, що вони беруть участь у формуванні кореневої системи, зокрема, в рості первинного та бічних коренів, їх густоти, розвитку адвентивних коренів, збільшенні густоти й довжини кореневих волосків. Водночас механізми транспорту стриголактонів від коренів до пагонів залишаються недослідженими. Стриголактони полегшують симбіоз рослини-хазяїна з актиноміцетами на рівні ризосфери. Окремо в огляді розглядається роль стриголактонів у формуванні надземної частини рослин — рості пазушних бруньок, розгалуженні стебла, рості міжвузлів, формуванні кутів розгалуження та рості стебел рослин, зубчастості листків. Відзначено, що роль стриголактонів у репродуктивному розвитку рослин досі залишається нез’ясованою, хоча в стриголактон-дефіцитних мутантів генеративні органи часто зменшені та деформовані. Крім того, стриголактони контролюють процеси цвітіння та бульбоутворення. Багатогранною є роль стриголактонів в адаптації рослин до дії стресових чинників, здебільшого до нестачі елементів мінерального живлення та осмотичного стресу. Окремо висвітлюється, що відкриття синтетичних аналогів стриголактонів створило можливості розробки нових агротехнологій контролювання бур’янів, хоча вони іноді мають низку недоліків, пов’язаних як з їх хімічними властивостями, так і з економічною доцільністю застосування цих аналогів. Розглядається взаємодія стриголактонів з іншими фітогормонами. Зокрема, синтез стриголактонів залежить від ауксинів, а в стриголактон-дефіцитних мутантів збільшується транспорт останніх. Водночас стриголактони та цитокініни здійснюють протилежний вплив на рослини на рівні багатьох фізіологічних процесів, наприклад, росту й розгалуження пагонів і старіння листків. Стриголактони й абсцизова кислота спільно координують механізми захисту рослин від дії посухи. Результати досліджень біологічної ролі стриголактонів і впливу їх синтетичних аналогів на рослинний організм можуть створити основу для розробки нових високопродуктивних агротехнологій.
Ключові слова: стриголактони, фітогормони, абіотичні чинники, рослина-паразит, рослина-хазяїн
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1. Zorrilla, J.G., Rial, C., Varela, R.M., Molinillo, J.M.G. & MacНas, F.A. (2022). Strategies for the synthesis of canonical, non-canonical and analogues of strigolactones, and evaluation of their parasitic weed germination activity. Phytochem. Rev., 21, рр. 1627-1659. https://doi.org/10.1007/s11101-022-09801-8
2. Cook, C.E., Whichard, L.P., Turner, B., Wall, M.E. & Egley, G.H. (1966). Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science, 154, pp. 1189-1190. https://doi.org/10.1126/science.154.3753.1189
3. Cook, C., Whichard, L.P., Wall, M., Egley, G.H., Coggon, P., Luhan, P.A. & McPhail, A. (1972). Germination stimulants. II. Structure of strigol, a potent seed germination stimulant for witchweed (Striga lutea). J. Am. Chem. Soc., 94, pp. 6198-6199. https://doi.org/10.1021/ja00772a048
4. Butler, L.G. (1995). Chemical communication between the parasitic weed striga and its crop host. ACS Symp. Ser., 582, pp. 158-168. https://doi.org/10.1021/bk-1995-0582.ch012
5. Dun, E.A., Brewer, P.B, Gillam, E.M.J. & Beveridge, C.A. (2023). Strigolactones and shoot branching: what is the real hormone and how does it work? Plant and Cell Physiol., 64 (9), pp. 967-983. https://doi.org/10.1093/pcp/pcad088
6. Rani, V., Sengar, R.S., Garg, S.K. & Mishra, P. (2023). Physiological and molecular role of strigolactones as plant growth regulators: a review. Mol. Biotech. https://doi.org/10.1007/s12033-023-00694-2
7. Akiyama, K, Matsuzaki, K.-I. & Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435, рр. 824-827. https://doi.org/10.1038/nature03608
8. Huralchuk, Zh.Z. & Morderer, Ye.Iu. (2023). Formuvannia arbuskuliarnoho mikoryznoho symbiozu i yoho vplyv na mozhlyvist infikuvannia roslynamy-parazytamy. Fakt. Eksper. Evol. Orhaniz., 33, pp. 176-179 [in Ukrainian]. https://doi.org/10.7124/FEEO.v33.1588
9. Zwanenburg, B. & Blanco-Ania, D. (2018). Strigolactones: new plant hormones in the spotlight. J. Exp. Bot., 69 (9), pp. 2205-2218. https://doi.org/10.1093/jxb/erx487
10. Aliche, E.B., Screpanti, C., De Mesmaeker, A., Munnik, T. & Bouwmeester, H.J. (2020). Science and application of strigolactones. New Phytol., 227, pp. 1001-1011. https://doi.org/10.1111/nph.16489
11. Bouwmeester, H.J., Fonne-Pfister, R., Screpanti, C. & De Mesmaeker, A. (2019). Strigolactones: plant hormones with promising features. Angew. Chem. Int. Ed., 58, 12778. https://doi.org/10.1016/j.plaphy.2023.108282
12. Shimels, M.Z., Rendine, S., Ruyter-Spira, C., Rich, P.J., Ejeta, G. & Bouwmeester, H.J. (2024). The role of strigolactone structural diversity in thehost specificity and control of Striga, a major constraint tosub-Saharan agriculture. Plants, People, Planet, pp. 1-13. https://doi.org/10.1002/ppp3.10549
13. Jia, K.P., Kountche B.A., Jamil, M., Guo, X., Ntui, V.O., Rтfenacht, A., Rochange, S. & Al-Babili, S. (2016). Nitro-phenlactone, a carlactone analog with pleiotropic strigolactone activities. Mol Plant, 9 (9), pp. 1341-1344. https://doi.org/10.1016/j.molp.2016.05.017
14. Nomura, T., Seto, Y. & Kyozuka, J. (2024). Unveiling the complexity of strigolactones: exploring structural diversity, biosynthesis pathways, and signaling mechanisms. J. Exp. Bot., 75 (4), pp. 1134-1147. https://doi.org/10.1093/jxb/erad412
15. Abe, S., Sado, A., Tanaka, K., Kisugi, T., Asami, K., Ota, S., Kim, H.I., Yoneyama, K., Xie, X. & Ohnishi, T. (2014). Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc. Natl. Acad. Sci. USA, 111, pp. 18084-18089. https://doi.org/10.1073/pnas.1410801111
16. Ueno, K., Furumoto, T., Umeda, S., Mizutani, M., Takikawa, H., Batchvarova, R. & Sugimoto, Y. (2014). Heliolactone, a non-sesquiterpene lactone germination stimulant for root parasitic weeds from sunflower. Phytochem., 108, pp. 122-128. https://doi.org/10.1016/j.phytochem.2014.09.018
17. Charnikhova, T.V., Gaus, K., Lumbroso, A., Sanders, M., Vincken, J-P., De Mesmaeker, A., Ruyter-Spira, C.P., Screpanti, C. & Bouwmeester, H.J. (2018). Zeapyranolactone - a novel strigolactone from maize. Phytochem. Lett, 24, рр. 172-178. https://doi.org/10.1016/j.phytol.2018.01.003
18. Xie, X., Kisugi, T., Yoneyama, K., Nomura, T., Akiyama, K., Uchida, K., Yokota, T., Christopher, S., McErlean, P. & Yoneyama, K. (2017). Methyl zealactonoate, a novel germination stimulant for root parasitic weeds produced by maize. J. Pestic. Sci., 42, рр. 58-61. https://doi.org/10.1584/jpestics.D16-103
19. Kim, H.I., Kisugi, T., Khetkam, P., Xie, X., Yoneyama, K., Uchida, K., Yokota, T., Nomura, T., McErlean, C.S. & Yoneyama, K. (2014). Avenaol, a germination stimulant for root parasitic plants from Avena strigosa. Phytochemistry, 103, рр. 85-88. https://doi.org/10.1016/j.phytochem.2014.03.030
20. Chesterfield, R.J., Vickers, C.E. & Beveridge, C.A. (2020). Translation of strigolactones from plant hormone to agriculture: achievements, future perspectives, and challenges. Trends Plant. Sci., 25 (11), pp. 1087-1106. https://doi.org/10.1016/j.tplants.2020.06.005
21. Jamil, M., Kanampiu, F.K., Karaya, H., Charnikhova, T. & Bouwmeester, H.J. (2012). Striga hermonthica parasitism in maize in response to N and P fertilisers. Field Crops Res., 134, рр. 1-10. https://doi.org/10.1016/j.fcr.2012.03.015
22. Mтller, S., Hauck, C. & Schildknecht, H. (1992). Germination stimulants produced by Vigna unguiculata Walp cv saunders upright. J. Plant. Growth Regul., 11, рр. 77-84. https://doi.org/10.1007/BF00198018
23. Yokota, T., Sakai, H., Okuno, K., Yoneyama, K. & Takeuchi, Y. (1998). Alectrol and orobanchol, germination stimulants for Orobanche minor, from its host red clover. Phytochem., 49 (7), pp. 1967-1973. https://doi.org/10.1016/S0031-9422(98)00419-1
24. Xie, X., Yoneyama, K., Kusumoto, D., Yamada, Y., Yokota, T., Takeuchi, Y. & Yoneyama, K. (2008). Isolation and identification of alectrol as (+)-orobanchyl acetate, a germination stimulant for root parasitic plants. Phytochem., 69 (2), pp. 427-431. https://doi.org/10.1016/j.phytochem.2007.07.017
25. Xie, X., Yoneyama, K., Kurita, J., Harada, Y., Yamada, Y., Takeuchi, Y. & Yoneyama, K. (2009). 7-oxoorobanchyl acetate and 7-oxoorobanchol as germination stimulants for root parasitic plants from flax (Linum usitatissimum). Biosci., Biotech. and Biochem., 73 (6), рр. 1367-1370. https://doi.org/10.1271/bbb.90021
26. Xie, X., Kusumoto, D., Takeuchi, Y., Yoneyama, K., Yamada, Y. & Yoneyama, K. (2007). 2¢-epi-orobanchol and solanacol, two unique strigolactones, germination stimulants for root parasitic weeds, produced by tobacco. J. Agricult. Food Chem., 55 (20), pp. 8067-8072. https://doi.org/10.1021/jf0715121
27. Xie, X., Yoneyama, K., Kisugi, T., Uchida, K., Ito, S., Akiyama, K., Hayashi, H., Takao, Y., Takahito, N. & Yoneyama, K. (2013). Confirming stereochemical structures of strigolactones produced by rice and tobacco. Molecul. Plant, 6 (1), pp. 153-163. https://doi.org/10.1093/mp/sss139
28. Tokunaga, T., Hayashi, H. & Akiyama, K. (2015). Medicaol, a strigolactone identified as a putative didehydro-orobanchol isomer, from Medicago truncatula. Phytochem., 111, pp. 91-97. https://doi.org/10.1016/j.phytochem.2014.12.024
29. ‡avar, S., Zwanenburg, B. & Tarkowski, P. (2015). Strigolactones: Occurrence, structure, and biological activity in the rhizosphere. Phytochem. Rev., 14, pp. 691-711. https://doi.org/10.1007/s11101-014-9370-4
30. Stirnberg, P, van De Sande, K. & Leyser, H.M. (2002). MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Develop., 129 (5), pp. 1131-1141. https://doi.org/10.1242/dev.129.5.1131
31. Waters, M.T., Gutjahr, C., Bennett, T. & Nelson, D. (2017). Strigolactone signalling and evolution. Annu. Rev. Plant Biol., 68, рр. 291-322. https://doi.org/10.1146/annurev-arplant-042916-040925
32. Xu, E., Chai, L., Zhang, S., Yu, R., Zhang, X., Xu, C. & Hu, Y. (2021). Catabolism of strigolactones by a carboxylesterase. Nature Plants, 7, pp. 1495-1504. https://doi.org/10.1038/s41477-021-01011-y
33. Guercio, A., Palayam, M. & Shabek, N. (2023). Strigolactones: diversity, perception, and hydrolysis. Phytochem. Rev., 22 (2), pp. 1-21. https://doi.org/10.1007/s11101-023-09853-4
34. Palayam, M., Yan, L., Nagalakshmi, U., Gilio, A.K., Cornu, D., Boyer, F-D., Dinesh-Kumar, S.P. & Shabek, N. (2024). Structural insights into strigolactone catabolism by carboxylesterases reveal a conserved conformational regulation. Nat. Commun., 15, 6500. https://doi.org/10.1038/s41467-024-50928-3
35. Yoneyama, K., Xie, X., Yoneyama, K., Kisugi, T., Nomura, T., Nakatani, Y., Akiyama, K. & McErlean, C.S.P. (2018). Which are the major players, canonical or non-canonical strigolactones? J. of Exp. Bot., 69 (9), pp. 2231-2239. https://doi.org/10.1093/jxb/ery090
36. Babiker, A.G.T., Ibrahim, N.E. & Edwards, W.G. (1988). Persistence of GR 7 and Striga germination stimulant(s) from Euphorbia aegyptiaca Boiss. in soils and in solutions. Weed Res., 28 (1), pp. 1-6. https://doi.org/10.1111/j.1365-3180.1988.tb00778.x
37. Mitra, D., Priyadarshini, A., Senapati, A., Behera, S., Chatterjee, I, Mohapatra, P.K.D. & Panneerselvam, P. (2023). Ecological importance of strigolactones hormone on arbuscular mycorrhizal fungi symbiosis in plant. Ind. J. Microbiol. Res., 9 (3), pp. 160-163. https://doi.org/10.18231/j.ijmr.2022.029
38. Halouzka, R., Zeljkoviє, S.‡., Boйivoj, K. & Tarkowski, P. (2020). Analytical methods in strigolactone research. Plant Meth. 16, 76. https://doi.org/10.1186/s13007-020-00616-2
39. Sun, H., Tao, J., Liu, S., Huang, S., Chen, S., Xie, X., Yoneyama, K., Zhang, Y. & Xu, G. (2014). Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J. Exp. Bot., 65, pp. 6735-6746. https://doi.org/10.1093/jxb/eru029
40. De Cuyper, C., Fromentin, J., Yocgo, R.E., De Keyser, A., Guillotin, B., Kunert, K., Boyer, F.D. & Goormachtig, S. (2015). From lateral root density to nodule number, the strigolactone analogue GR24 shapes the root architecture of Medicago truncatula. J. Exp. Bot., 66, pp. 137-146. https://doi.org/10.1093/jxb/erv227
41. Olah, D., Feigl, G., Molnar, A., љrdШg, A. & Kolbert, Z. (2020). Strigolactones interact with nitric oxide in regulating root system architecture of Arabidopsis thaliana. Front. Plant Sci., 11, 1019. https://doi.org/10.3389/fpls.2020.01019
42. Matthys, C., Walton, A., Struk, S., Stes, E., Boyer, F.D., Gevaert, K. & Goormachtig, S. (2016). The whats, the wheres and the hows of strigolactone action in the roots. Planta, 243 (6), pp. 1327-1337. https://doi.org/10.1007/s00425-016-2483-9
43. Soundappan, I., Bennett, T., Morffy, N., Liang, Y., Stanga, J.P., Abbas, A., Leyser, O. & Nelson, D.C. (2015). SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell, 27, pp. 3143-3159. https://doi.org/10.1105/tpc.15.00562
44. Li, S., Chen, L., Li, Y., Yao, R., Wang, F., Yang, M., Gu, M., Nan, F., Xie, D. & Yan, J. (2016). Effect of GR24 stereoisomers on plant development in Arabidopsis. Mol. Plant, 9, pp. 1432-1435. https://doi.org/10.1016/j.molp.2016.06.012
45. Rasmussen, A., Mason, M.G., De Cuyper, C., Brewer, P.B., Herold, S., Agusti, J., Geelen, D., Greb, T., Goormachtig, S., Beeckman, T. & Beveridge, C.A. (2012). Strigolactones suppress adventitious rooting in Arabidopsis and pea. Plant Physiol., 158, pp. 1976-1987. https://doi.org/10.1104/pp.111.187104
46. Sun, H., Tao, J., Hou, M., Huang, S., Chen, S., Liang, Z., Xie, T., Wei, Y., Xie, X., Yoneyama, K., Xu, G. & Zhang, Y. (2015). A strigolactone signal is required for adventitious root formation in rice. Ann. Bot., 115, pp. 1155-1162. https://doi.org/10.1093/aob/mcv052
47. Mayzlish-Gati, E., De-Cuyper, C., Goormachtig, S., Beeckman, T., Vuylsteke, M., Brewer, P.B., Beveridge, C.A., Yermiyahu, U., Kaplan, Y., Enzer, Y., Wininger, S., Resnick, N., Cohen, M., Kapulnik, Y. & Koltai, H. (2012). Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol., 160, pp. 1329-1341. https://doi.org/10.1104/pp.112.202358
48. Ito, S., Nozoye, T., Sasaki, E., Imai, M., Shiwa, Y., Shibata-Hatta, M., Ishige, T., Fukui, K., Ito, K., Nakanishi, H., Nishizawa, N.K., Yajima, S. & Asami, T. (2015). Strigolactone regulates anthocyanin accumulation, acid phosphatases production and plant growth under low phosphate condition in Arabidopsis. PLoS One, 10, e0119724. https://doi.org/10.1371/journal.pone.0119724
49. Li, S., Chen, L., Li, Y., Yao, R., Wang, F., Yang, M., Gu, M., Nan, F., Xie, D. & Yan, J. (2016). Effect of GR24 stereoisomers on plant development in Arabidopsis. Mol. Plant, 9, pp. 1432-1435. https://doi.org/10.1016/j.molp.2016.06.012
50. Kohlen, W., Charnikhova, T., Liu, Q., Bours, R., Domagalska, M.A., Beguerie, S., Verstappen, F., Leyser, O., Bouwmeester, H.J., Ruyter-Spira, C. (2011). Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in non-AM host Arabidopsis thaliana. Plant Physiol., 110, 164640. https://doi.org/10.1104/pp.110.164640
51. Xie, X., Yoneyama, K., Kisugi, T., Nomura, T., Akiyama, K., Asami, T. & Yoneyama, K. (2015). Strigolactones are transported from roots to shoots, although not through the xylem. J. Pestic. Sci., 40, pp. 214-216. https://doi.org/10.1584/jpestics.D15-045
52. Huralchuk, Zh.Z. (2010). Diia arbuskuliarnykh mikoryz na nadkhodzhennia elementiv zhyvlennia i stiikist roslyn do nespryiatlyvykh chynnykiv dovkillia. Silskohospodarska Mikrobiol., 12, pp. 7-26 [in Ukrainian]. https://doi.org/10.35868/1997-3004.12.7-26
53. De Saint Germain, A., Ligerot, Y., Dun, E.A., Pillot, J-PJ-P., Ross, J.J., Beveridge, C.A. & Rameau, C. (2013). Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol., 163, pp. 1012-1025. https://doi.org/10.1104/pp.113.220541
54. Lauressergues, D., Andrѕ, O., Peng, J., Wen, J., Chen, R., Ratet, P., Tadege, M., Mysore, K.S. & Rochange, S.F. (2015). Strigolactones contribute to shoot elongation and to the formation of leaf margin serrations in Medicago truncatula R108. J. Exp. Bot., 66, pp. 1237-1244. https://doi.org/10.1093/jxb/eru471
55. Liang, Y., Ward, S., Li, P., Bennett, T. & Leyser, O. (2016). SMAX1-LIKE7 signals from the nucleus to regulate shoot development in Arabidopsis via partially EAR motif-independent mechanisms. Plant Cell., 28, pp. 1581-1601. https://doi.org/10.1105/tpc.16.00286
56. Shindo, M., Yamamoto, S., Shimomura, K. & Umehara, M. (2020). Strigolactones decrease leaf angle in response to nutrient deficiencies in rice. Front. Plant Sci., 11, 135. https://doi.org/10.3389/fpls.2020.00135
57. Agusti, J., Herold, S., Schwarza, M., Sanchez, P., Ljung, K., Dun, E.A., Brewer, P.B., Beveridge, C.A., Siebererd, T., Sehra, E.M. & Greb, T. (2011). Strigolactone signalling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl. Acad. Sci. USA, 108, pp. 20242-20247. https://doi.org/10.1073/pnas.1111902108
58. Soundappan, I., Bennett, T., Morffy, N., Liang, Y., Stanga, J.P., Abbas, A., Leyser, O. & Nelson, D.C. (2015). SMAX1-LIKE/D53 family members enable distinct MAX2-dependent responses to strigolactones and karrikins in Arabidopsis. Plant Cell, 27, pp. 3143-3159. https://doi.org/10.1105/tpc.15.00562
59. Scaffidi, A., Waters, M.T., Sun, Y.K., Skelton, B.W., Dixon, K.W., Ghisalberti, E.L., Flematti, G.R. & Smith, S.M. (2014). Strigolactone hormones and their stereoisomers signal through two related receptor proteins to induce different physiological responses in Arabidopsis. Plant Physiol., 165 (3), рр. 1221-1232. https://doi.org/10.1104/pp.114.240036
60. Bainbridge, K., Sorefan, K., Ward, S. & Leyser, O. (2005). Hormonally MAX4 shoot branching regulatory gene. Plant J., 44, pp. 569-580. https://doi.org/10.1111/j.1365-313X.2005.02548.x
61. Vogel, J.T., Walter, M.H., Giavalisco, P., Lytovchenko, A., Kohlen, W., Charnikhova, T., Simkin, A.J., Goulet, C., Strack, D., Bouwmeester, H.J., Fernie, A.R. & Klee, H.J. (2010). SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J., 61, pp. 300-311. https://doi.org/10.1111/j.1365-313X.2009.04056.x
62. Kohlen, W., Charnikhova, T., Lammers, M., Pollina T., TЩth P., Haider I., Pozo, M.J., de Maagd R.A., Ruyter-Spira, C., Bouwmeester, H.J. & LЩpez-R«ez, J.A. (2012). The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 196, pp. 535-547. https://doi.org/10.1111/j.1469-8137.2012.04265.x
63. Dingenen, J.V., Keyser, A., Desmet, S., Clarysse, A., Beullens, S., Michiels, J., Planque, M. & Goormachtig, S. (2023). Strigolactones repress nodule development and senescence in pea. Plant J., 116, pp. 7-22. https://doi.org/10.1111/tpj.16421
64. Snowden, K.C., Simkin, A.J., Janssen, B.J., Templeton, K.R., Loucas, H.M., Simons, J.L., Karunairetnam, S., Gleave, A.P., Clark, D.G. & Klee, H.J. (2005). The decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell, 17, pp. 746-759. https://doi.org/10.1105/tpc.104.027714
65. Visentin, I., Ferigolo, L.F., Russo, G., Korwin Krukowski, P., Capezzali, C., Tarkowsk«, D., Gresta, F., Deva, E., Nogueira, F.T.S., Schubert, A. & Cardinale, F. (2024). Strigolactones promote flowering by inducing the miR319-LA-SFT module in tomato. Proc. Natl. Acad. Sci. USA, 121 (19), e2316371121. https://doi.org/10.1073/pnas.2316371121
66. Alvi, A.F., Sehar, Z., Fatma, M., Masood, A. & Khan, N.A. (2022). Strigolactone: An emerging growth regulator for developing resilience in plants. Plants, 11 (19), 2604. https://doi.org/10.3390/plants11192604
67. Kapoor, R.T., Alam, P., Chen, Y., Chen, Y. & Ahmad, P. (2024). Strigolactones in plants: from development to abiotic stress management. J. Plant Growth Regul., 43 (4), pp. 903-919. https://doi.org/10.1007/s00344-023-11148-z
68. Khalid, M.F., Shafqat, W., Khan, R.I., Jawaid, M.Z., Hussain, S., Saqib, M., Rizwan, M. & Ahmed, T. (2024). Unveiling the resilience mechanism: Strigolactones as master regulators of plant responses to abiotic stresses. Plant Stress, 12, 100490. https://doi.org/10.1016/j.stress.2024.100490
69. Khan, M.K., Pandey, A., Hamurcu, M., Vyhn«nek, T., Zargar, S.M., Kahraman, A., Topal, A. & Gezgin, S. (2024). Exploring strigolactones for inducing abiotic stress tolerance in plants. Czech J. Genet. Plant Breed., 60 (2), pp. 55-69. https://doi.org/10.17221/88/2023-CJGPB
70. Trasoletti, M., Visentin, I., Campo, E., Schubert, A. & Cardinale, F. (2022). Strigolactones as a hormonal hub for the acclimation and priming to environmental stress in plants. Plant Cell Environ., 45, pp. 3611-3630. https://doi.org/10.1111/pce.14461
71. Soliman, S., Wang, Y., Han, Z., Pervaiz, T. & El-Kereamy, A. (2022). Strigolactones in plants and their interaction with the ecological microbiome in response to abiotic stress. Plants, 11, 3499. https://doi.org/10.3390/plants11243499
72. Lopez-Raez, J.A., Shirasu, K. & Foo, E. (2017). Strigolactones in plant interactions with beneficial and detrimental organisms: the Yin and Yang. Trends Plant Sci., 22, рр. 527-537. https://doi.org/10.1016/j.tplants.2017.03.011
73. Santoro, V., Schiavon, M., Gresta, F., Ertani, A., Cardinale, F., Sturrock, C.J., Celi, L. & Schubert, A. (2020). Strigolactones control root system architecture and tip anatomy in Solanum lycopersicum L. plants under P starvation. Plants, 9 (5), 612. https://doi.org/10.3390/plants9050612
74. Lanfranco, L., Fiorilli, V., Venice, F. & Bonfante, P. (2018). Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J. Exp. Bot., 69, pp. 2175-2188. https://doi.org/10.1093/jxb/erx432
75. Breuillin, F., Schramm, J., Hajirezaei, M., Ahkami, A., Favre, P., Druege, U., Hause, B., Bucher, M., Kretzschmar, T. & Bossolini, E. (2010). Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J., 64, pp. 1002-1017. https://doi.org/10.1111/j.1365-313X.2010.04385.x
76. Asad, N.M., Zhang, Z.Q., Mukhtar, A., Muhammad, S.A., Wu, H.Y., Yang, H. & Zhou, X.B. (2024). Strigolactones: A promising tool for nutrient acquisition through arbuscular mycorrhizal fungi symbiosis and abiotic stress tolerance. Plant Physiol. Biochem., 215, 109057. https://doi.org/10.1016/j.plaphy.2024.109057
77. Jiang, W., Lu, C., Xu, X., Riaz, M.W., Aimin, L.V. & Shao, Q. (2024). Strigolactones: Biosynthetic regulation, hormonal interaction, and their involvement in abiotic stress adaption. Scientia Horticult., 325, 112689. https://doi.org/10.1016/j.scienta.2023.112689
78. Ito, S., Ito, K., Abeta, N., Takahashi, R., Sasaki, Y. & Yajima, S. (2016). Effects of strigolactone signalling on Arabidopsis growth under nitrogen deficient stress condition. Plant Signal Behav., 11, e1126031. https://doi.org/10.1080/15592324.2015.1126031
79. Umehara, M., Hanada, A., Magome, H., Takeda-Kamiya, N. & Yamaguchi, S. (2010). Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol., 51, pp. 1118-1126. https://doi.org/10.1093/pcp/pcq084
80. Yamada, Y., Furusawa, S., Nagasaka, S., Shimomura, K., Yamaguchi, S. & Umehara, M. (2014). Strigolactone signalling regulates rice leaf senescence in response to a phosphate deficiency. Planta, 240, pp. 399-408. https://doi.org/10.1007/s00425-014-2096-0
81. Linkohr, B.I., Williamson, L.C., Fitter, A.H. & Leyser, H.M. (2002). Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J., 29, pp. 751-760. https://doi.org/10.1046/j.1365-313X.2002.01251.x
82. Lynch, J.P. & Brown, K.M. (2001). Topsoil foraging - an architectural adaptation of plants to low phosphorus availability. Plant Soil, 237, pp. 225-237. https://doi.org/10.1023/A:1013324727040
83. Madmon, O., Mazuz, M., Kumari, P., Dam, A., Ion, A., Mayzlish-Gati, E., Belausov, E., Wininger, S., Abu-Abied, M., McErlean, C.S., Bromhead, L.J, Perl-Treves, R., Prandi, C., Kapulnik, Y. & Koltai, H. (2016). Expression of MAX2 under SCARECROW promoter enhances the strigolactone/MAX2 dependent response of Arabidopsis roots to low-phosphate conditions. Planta, 243, pp. 1419-1427. https://doi.org/10.1007/s00425-016-2477-7
84. Mayzlish-Gati, E., De-Cuyper, C., Goormachtig, S., Beeckman, T., Vuylsteke, M., Brewer, P.B., Beveridge, C.A., Yermiyahu, U., Kaplan, Y., Enzer, Y., Wininger, S., Resnick, N., Cohen, M., Kapulnik, Y. & Koltai, H. (2012). Strigolactones are involved in root response to low phosphate conditions in Arabidopsis. Plant Physiol., 160, pp. 1329-1341. https://doi.org/10.1104/pp.112.202358
85. Alsubaie, Q.D., Al-Amri, A.A., Siddiqui, M.H. & Alamri, S. (2024). Strigolactone and nitric oxide collaborate synergistically to boost tomato seedling resilience to arsenic toxicity via modulating physiology and the antioxidant system. Plant Physiol. and Biochem., 108412. https://doi.org/10.1016/j.plaphy.2024.108412
86. Liu, J., He, H., Vitali, M., Visentin, I., Charnikhova, T., Haider, I., Schubert, A., Ruyter-Spira, C., Bouwmeester, H.J., Lovisolo, C. & Cardinale, F. (2015). Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta, 241, pp. 1435-1451. https://doi.org/10.1007/s00425-015-2266-8
87. Lv, S., Zhang, Y., Li, C., Liu, Z., Yang, N., Pan, L., Wu, J., Wang, J., Yang, J., Lv, Y., Zhang, Y., Jiang, W., She, X. & Wang, G. (2018). Strigolactone-triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytol., 217, pp. 290-304. https://doi.org/10.1111/nph.14813
88. Zhong, L., Yang, C., Chen, Y., Guo, L., Liu, D., Deng, J., Xu, Y., Chen, Y. & Zhao, D. (2024). Reduced strigolactone synthesis weakens drought resistance in tall fescue via root development inhibition. Agronomy, 14 (4), 725. https://doi.org/10.3390/agronomy14040725
89. Borase, H.P., Patil, S.V. & Amin, D. (2022). Strigolactones: Extraction and Characterization. In: Practical handbook on agricultural microbiology. Amaresan, N., Patel, P. & Amin, D. (Eds.). Springer Protocols Handbooks. New York: Humana, NY. https://doi.org/10.1007/978-1-0716-1724-3_38
90. Vurro, M., Prandib, C. & Baroccio, F. (2016). Strigolactones: how far is their commercial use for agricultural purposes? Pest Manag. Sci., 72 (11), pp. 2009-2187. https://doi.org/10.1002/ps.4254
91. Johnson, A.W., Gowada, G., Hassanali, A., Knox, J., Monaco, S., Razavi, Z. & Rosebery, G. (1981). The preparation of synthetic analogues of strigol, J. Chem. Soc. Perkin Trans., 1, рр. 1734-1743. https://doi.org/10.1039/p19810001734
92. Nefkens, G.H.L., Thuring, J.W.J.F., Beenakkers, M.F.M. & Zwanenburg, B. (1997). Synthesis of a phthaloylglycine-derived strigol analogue and its germina- tion stimulatory activity toward seeds of the parasitic weeds Striga hermonthica and Orobanche crenata, J. Agric. Food Chem., 45, рр. 2273-2277. https://doi.org/10.1021/jf9604504
93. Kondo, Y., Tadokoro, E., Matsuura, M., Iwasaki, K., Sugimoto, Y., Miyake, H., Takikawa, H. & Sasaki, M. (2007). Synthesis and seed germination stimulating activity of some iminoanalogs of strigolactones. Biosci. Biotech. Biochem., 71 (11), pp. 2781-2786. https://doi.org/10.1271/bbb.70398
94. Cetin, E.S. & Koc, B. (2022). The effects of strigolactones on some biochemical traits in calcified media on grapevine. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 50 (4), 12816. https://doi.org/10.15835/nbha50312816
95. Song, M., Zhou, S., Hu, N., Li, J., Huang, Y., Zhang, J., Chen, X., Du, X., Niu, J., Yang, X. & He, D. (2023). Exogenous strigolactones alleviate drought stress in wheat (Triticum aestivum L.) by promoting cell wall biogenesis to optimize root architecture. Plant Physiol. and Biochem., 204, 108121. https://doi.org/10.1016/j.plaphy.2023.108121
96. Fukui, K., Ito, S., Ueno, K., Yamaguchi, S., Junko, K. & Asami, T. (2011). New branching inhibitors and their potential as strigolactone mimics in rice. Bioorg. Med. Chem. Lett., 21 (16), pp. 4905-4908. https://doi.org/10.1016/j.bmcl.2011.06.019
97. Zwanenburg, B. & Mwakaboko, A.S. (2011). Strigolactone analogues and mimics derived from phthalimide, saccharine, p-tolylmalondialdehyde, benzoic and salicylic acid as scaffolds. Bioorg. Med. Chem., 19 (24), pp. 7394-7400. https://doi.org/10.1016/j.bmc.2011.10.057
98. Boyer, F-D., de Saint Germain, A., Pillot, J-P., Pouvreau, J-B., Chen, X., Ramos, S., Stѕvenin, A., Simier, P., Delavault, P., Beau, J-M. & Rameau, C. (2012). Structure-activity relationship studies of strigolactone-related molecules for branching inhibition in garden pea: molecule design for shoot branching. Plant Physiol., 159 (4), pp. 1524-1544. https://doi.org/10.1104/pp.112.195826
99. Xie, X., Yoneyama, K. & Yoneyama, K. (2010). The strigolactone story. Annu. Rev. Phytopathol., 48, pp. 93-117. https://doi.org/10.1146/annurev-phyto-073009-114453
100. Prandi, C. & McErlean, C.S.P. (2019). The chemistry of strigolactones. In: Strigolactones - biology and applications. Koltai, H. & Prandi, C. (Eds.). Switzerland, Cham: Springer Nature. https://doi.org/10.1007/978-3-030-12153-2
101. Soto-Cruz, F.J., Zorrilla, J.G. & Rial, C. (2021). Allelopathic activity of strigolactones on the germination of parasitic plants and arbuscular mycorrhizal fungi growth. Agronomy, 11, е2174. https://doi.org/10.3390/agronomy11112174
102. Zwanenburg, B., Mwakaboko, A.S. & Kannana, C. (2016). Suicidal germination for parasitic weed control. Pest. Manag. Sci., 72 (11), pp. 2016-2025. https://doi.org/10.1002/ps.4222
103. Eplee, R.E. (1984). Chemical control of Striga. In: Striga. Biology and control. Ayensu, E.S., Doggett, H. & Keynes, R.D. (Eds.). Paris: ICSU Press; Ottawa: Int. Res. Development Centre. https://doi.org/ 10.1017/S0014479700013302
104. Ogborn, J. (1984). Striga: research priorieties with specific reference to agronomy. In: Striga. Biology and control. Ayensu, E.S., Doggett, H. & Keynes, R.D. (Eds.). Paris: ICSU Press; Ottawa: Int. Res. Development Centre. https://doi.org/10.1017/ S0014479700013302
105. Johnson, X., Brcich, T., Dun, E.A., Goussot, M., Haurognѕ, K., Beveridge, C.A. & Rameau, C. (2006). Branching genes are conserved across species. Genes controlling a novel signal in pea are coregulated by other long-distance signals. Plant Physiol., 142, pp. 1014-1026. https://doi.org/10.1104/pp.106.087676
106. Wu, F., Gao, Y., Yang, W., Sui, N. & Zhu, J. (2022). Biological functions of strigolactones and their crosstalk with other phytohormones. Front Plant Sci., 13, 821563. https://doi.org/10.3389/fpls.2022.821563
107. Arite, T., Iwata, H., Ohshima, K., Maekawa, M., Nakajima, M., Kojima, M., Sakakibara, H. & Kyozuka, J. (2007). DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J., 51, pp. 1019-1029. https://doi.org/10.1111/j.1365-313X.2007.03210.x
108. Hayward, A., Stirnberg, P., Beveridge, C. & Leyser, O. (2009). Interactions between auxin and strigolactone in shoot branching control. Plant Physiol., 151, pp. 400-412. https://doi.org/10.1104/pp.109.137646
109. Trasoletti, M., Visentin, I., Campo, E., Schubert, A. & Cardinale, F. (2022). Strigolactones as a hormonal hub for the acclimation and priming to environmental stress in plants. Plant Cell Environ., 45, pp. 3611-3630. https://doi.org/10.1111/pce.14461
110. Adamowski, M. & Friml, J. (2015). PIN-dependent auxin transport: action, regulation, and evolution. The Plant Cell, 27 (1), pp. 20-32. https://doi.org/10.1105/tpc.114.134874
111. Beveridge, C.A., Symons, G.M. & Turnbull, C.G. (2000). Auxin inhibition of decapitation-induced branching is dependent on graft-transmissible signals regulated by genes Rms1 and Rms2. Plant Physiol., 123, pp. 689-698. https://doi.org/10.1104/pp.123.2.689
112. Shinohara, N., Taylor, C. & Leyser, O. (2013). Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol, 11, e1001474. https://doi.org/10.1371/journal.pbio.1001474
113. Seale, M., Bennett, T. & Leyser, O. (2017). BRC1 expression regulates bud activation potential but is not necessary or sufficient for bud growth inhibition in Arabidopsis. Dev., 144, pp. 1661-1673. https://doi.org/10.1242/dev.145649
114. Xu, Y., Ge, J., Tian, S., Li, S., Nguy-Robertson, A.L., Zhan, M. & Cao, C. (2015). Effects of water-saving irrigation practices and drought resistant rice variety on greenhouse gas emissions from a no-till paddy in the central lowlands of China. Sci Total Environ., 505, pp. 1043-1052. https://doi.org/10.1016/j.scitotenv.2014.10.073
115. Wallner, E.S., LЩpez-SalmerЩn, V. & Greb, T. (2016). Strigolactone versus gibberellin signalling: reemerging concepts? Planta, 243, pp. 1339-1350. https://doi.org/10.1007/s00425-016-2478-6
116. Ito, S., Yamagami, D., Umehara, M., Hanada, A., Yoshida, S., Sasaki, Y., Yajima, S., Kyozuka, J., Ueguchi-Tanaka, M. & Matsuoka, M. (2017). Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol., 174, pp. 1250-1259. https://doi.org/10.1104/pp.17.00301
117. Lantzouni, O., Klermund, C. & Schwechheimer, C. (2017). Largely additive effects of gibberellin and strigolactone on gene expression in Arabidopsis thaliana seedlings. Plant J., 92, pp. 924-938. https://doi.org/10.1111/tpj.13729
118. Korek, M. & Marzec, M. (2023). Strigolactones and abscisic acid interactions affect plant development and response to abiotic stresses. BMC Plant Biol., 23, 314. https://doi.org/10.1186/s12870-023-04332-6
119. Lopez-Raez, J.A. (2016). How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta, 243, pp. 1375-1385. https://doi.org/10.1007/s00425-015-2435-9