Abstract
Strigolactones (SLs), a class of carotenoid-derived phytohormones, were originally discovered as rhizosphere signaling molecules. They stimulate parasitic plant seed germination and can establish a symbiotic relationship between plants and beneficial microbes. In addition to their plant developmental role, evidence for their role in various stress responses such as salt and drought stresses was reported recently. In the present study, we tried to understand the unique metabolic pathways that were regulated by SLs in comparison with other plant hormones. We identified that SLs were predominantly modulating photosynthetic pathways in comparison with other plant hormones. Further, we observed that SLs positively influence high light tolerance, and this process is dependent on SL-mediated photosynthesis rate regulation. In addition, the dynamic changes of the metabolites involved in glycolysis and tricarboxylic acid (TCA) cycle upon external application of SL analogue suggest the stress adaptation landscape of plants. Our study presents the dynamic and specific effect of SLs in high light-driven stress adaptation through photosynthesis in plants.
This is a preview of subscription content, access via your institution.






Data Availability
The raw data files of the transcriptome data are available in Array Express, EBI, under the accession number E-MTAB-11329. All the other data used in the analysis were provided in the supplementary information.
References
Akiyama K, Matsuzaki K-i, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435(7043):824–827
Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335(6074):1348–1351
Alexander A, Singh VK, Mishra A, Jha B (2019) Plant growth promoting rhizobacterium Stenotrophomonas maltophilia BJ01 augments endurance against N2 starvation by modulating physiology and biochemical activities of Arachis hypogea. PLoS ONE 14(9):e0222405. https://doi.org/10.1371/journal.pone.0222405
Anand David AV, Arulmoli R, Parasuraman S (2016) Overviews of biological importance of quercetin: a bioactive flavonoid. Pharmacogn Rev 10(20):84–89. https://doi.org/10.4103/0973-7847.194044
Anders S, Pyl PT, Huber W (2015) HTSeq–a Python framework to work with high-throughput sequencing data. Bioinformatics 31(2):166–169. https://doi.org/10.1093/bioinformatics/btu638
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50(8):1416–1424. https://doi.org/10.1093/pcp/pcp091
Aroca R, Ruiz-Lozano JM, Zamarreño ÁM, Paz JA, García-Mina JM, Pozo MJ, López-Ráez JA (2013) Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J Plant Physiol 170(1):47–55
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. J Exp Bot 55(403):1607–1621. https://doi.org/10.1093/jxb/erh196
Batista-Silva W, Heinemann B, Rugen N, Nunes-Nesi A, Araujo WL, Braun HP, Hildebrandt TM (2019) The role of amino acid metabolism during abiotic stress release. Plant Cell Environ 42(5):1630–1644. https://doi.org/10.1111/pce.13518
Bennett T, Sieberer T, Willett B, Booker J, Luschnig C, Leyser O (2006) The Arabidopsis MAX pathway controls shoot branching by regulating auxin transport. Curr Biol 16(6):553–563. https://doi.org/10.1016/j.cub.2006.01.058
Berka M, Luklova M, Dufkova H, Berkova V, Novak J, Saiz-Fernandez I, Rashotte AM, Brzobohaty B, Cerny M (2020) Barley root proteome and metabolome in response to cytokinin and abiotic stimuli. Front Plant Sci 11:590337. https://doi.org/10.3389/fpls.2020.590337
Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais J-C, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4(7):e226
Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8(3):443–449
Bown AW, Shelp BJ (2016) Plant GABA: not just a metabolite. Trends Plant Sci 21(10):811–813. https://doi.org/10.1016/j.tplants.2016.08.001
Brewer PB, Dun EA, Ferguson BJ, Rameau C, Beveridge CA (2009) Strigolactone acts downstream of auxin to regulate bud outgrowth in pea and Arabidopsis. Plant Physiol 150(1):482–493. https://doi.org/10.1104/pp.108.134783
Brewer PB, Yoneyama K, Filardo F, Meyers E, Scaffidi A, Frickey T, Akiyama K, Seto Y, Dun EA, Cremer JE (2016) Lateral branching oxidoreductase acts in the final stages of strigolactone biosynthesis in Arabidopsis. Proc Natl Acad Sci 113(22):6301–6306
Cardoso C, Zhang Y, Jamil M, Hepworth J, Charnikhova T, Dimkpa SO, Meharg C, Wright MH, Liu J, Meng X, Wang Y, Li J, McCouch SR, Leyser O, Price AH, Bouwmeester HJ, Ruyter-Spira C (2014) Natural variation of rice strigolactone biosynthesis is associated with the deletion of two MAX1 orthologs. Proc Natl Acad Sci USA 111(6):2379–2384. https://doi.org/10.1073/pnas.1317360111
Ćavar S, Zwanenburg B, Tarkowski P (2014) Strigolactones: occurrence, structure, and biological activity in the rhizosphere. Phytochem Rev 14(4):691–711. https://doi.org/10.1007/s11101-014-9370-4
Choudhury S, Sharma P, Moulick D, Mazumder MK (2021) Unrevealing metabolomics for abiotic stress adaptation and tolerance in plants. J Crop Sci Biotechnol. https://doi.org/10.1007/s12892-021-00102-8
Coleto I, Pineda M, Rodiño A, De Ron A, Alamillo J (2014) Comparison of inhibition of N2 fixation and ureide accumulation under water deficit in four common bean genotypes of contrasting drought tolerance. Ann Bot 113(6):1071–1082
Crawford S, Shinohara N, Sieberer T, Williamson L, George G, Hepworth J, Muller D, Domagalska MA, Leyser O (2010) Strigolactones enhance competition between shoot branches by dampening auxin transport. Development 137(17):2905–2913. https://doi.org/10.1242/dev.051987
David AVA, Arulmoli R, Parasuraman S (2016) Overviews of biological importance of quercetin: a bioactive flavonoid. Pharmacogn Rev 10(20):84
Delaux PM, Xie X, Timme RE, Puech-Pages V, Dunand C, Lecompte E, Delwiche CF, Yoneyama K, Bécard G, Séjalon-Delmas N (2012) Origin of strigolactones in the green lineage. New Phytol 195(4):857–871
Diagne N, Ngom M, Djighaly PI, Fall D, Hocher V, Svistoonoff S (2020) Roles of arbuscular mycorrhizal fungi on plant growth and performance: importance in biotic and abiotic stressed regulation. Diversity 12(10):370
Dumschott K, Richter A, Loescher W, Merchant A (2017) Post photosynthetic carbon partitioning to sugar alcohols and consequences for plant growth. Phytochemistry 144:243–252. https://doi.org/10.1016/j.phytochem.2017.09.019
Erickson E, Wakao S, Niyogi KK (2015) Light stress and photoprotection in Chlamydomonas reinhardtii. Plant J 82(3):449–465. https://doi.org/10.1111/tpj.12825
Fankhauser C, Christie JM (2015) Plant phototropic growth. Curr Biol 25(9):R384-389. https://doi.org/10.1016/j.cub.2015.03.020
Fernandez O, Bethencourt L, Quero A, Sangwan RS, Clement C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15(7):409–417. https://doi.org/10.1016/j.tplants.2010.04.004
Finlayson SA, Krishnareddy SR, Kebrom TH, Casal JJ (2010) Phytochrome regulation of branching in Arabidopsis. Plant Physiol 152(4):1914–1927
Foo E, Bullier E, Goussot M, Foucher F, Rameau C, Beveridge CA (2005) The branching gene RAMOSUS1 mediates interactions among two novel signals and auxin in pea. Plant Cell 17(2):464–474. https://doi.org/10.1105/tpc.104.026716
Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Ann Bot 96(2):169–175. https://doi.org/10.1093/aob/mci165
Gangola MP, Ramadoss BR (2018) Sugars play a critical role in abiotic stress tolerance in plants. In Biochemical, physiological and molecular avenues for combating abiotic stress tolerance in plants. Elsevier, pp 17–38
Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li W, Ogawa M, Yamauchi Y, Preston J, Aoki K, Kiba T, Takatsuto S, Fujioka S, Asami T, Nakano T, Kato H, Mizuno T, Sakakibara H, Yamaguchi S, Nambara E, Kamiya Y, Takahashi H, Hirai MY, Sakurai T, Shinozaki K, Saito K, Yoshida S, Shimada Y (2008) The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant J 55(3):526–542. https://doi.org/10.1111/j.1365-313X.2008.03510.x
Godoy F, Olivos-Hernandez K, Stange C, Handford M (2021) Abiotic stress in crop species: improving tolerance by applying plant metabolites. Plants (Basel). https://doi.org/10.3390/plants10020186
Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot J-P, Letisse F, Matusova R, Danoun S, Portais J-C (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194
Guidi L, Tattini M, Landi M (2017) Chlorophyll. In: Jacob-Lopes Eduardo, Zepka Leila Queiroz, Queiroz Maria Isabel (eds) How does chloroplast protect chlorophyll against excessive light? InTech
Gururani MA, Venkatesh J, Tran LS (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8(9):1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
Hamiaux C, Drummond RS, Janssen BJ, Ledger SE, Cooney JM, Newcomb RD, Snowden KC (2012) DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone. Curr Biol 22(21):2032–2036
Hasan M, Alabdallah NM, Alharbi BM, Waseem M, Yao G, Liu X-D, El-Gawad A, Hany G, El-Yazied AA, Ibrahim MF (2021) GABA: a key player in drought stress resistance in plants. Int J Mol Sci 22(18):10136
Hayward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151(1):400–412. https://doi.org/10.1104/pp.109.137646
Huang H, Ullah F, Zhou D-X, Yi M, Zhao Y (2019) Mechanisms of ROS regulation of plant development and stress responses. Front Plant Sci. https://doi.org/10.3389/fpls.2019a.00800
Huang J, Zhao X, Chory J (2019) The Arabidopsis transcriptome responds specifically and dynamically to high light stress. Cell Rep 29(12):4186–4199. https://doi.org/10.1016/j.celrep.2019b.11.051
Jespersen D, Yu J, Huang B (2017) Metabolic effects of acibenzolar-s-methyl for improving heat or drought stress in creeping bentgrass. Front Plant Sci 8:1224. https://doi.org/10.3389/fpls.2017.01224
Jia KP, Luo Q, He SB, Lu XD, Yang HQ (2014) Strigolactone-regulated hypocotyl elongation is dependent on cryptochrome and phytochrome signaling pathways in Arabidopsis. Mol Plant 7(3):528–540. https://doi.org/10.1093/mp/sst093
Jin H, Li M, Duan S, Fu M, Dong X, Liu B, Feng D, Wang J, Wang HB (2016) Optimization of light-harvesting pigment improves photosynthetic efficiency. Plant Physiol 172(3):1720–1731. https://doi.org/10.1104/pp.16.00698
Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420(6917):829–832
Kaur H, Chowrasia S, Gaur VS, Mondal TK (2021) Allantoin: emerging role in plant abiotic stress tolerance. Plant Mol Biol Report 39(3):648–661. https://doi.org/10.1007/s11105-021-01280-z
Kim G-T, Yano S, Kozuka T, Tsukaya H (2005) Photomorphogenesis of leaves: shade-avoidance and differentiation of sun and shade leaves. Photochem Photobiol Sci 4(9):770–774
Kleine T, Kindgren P, Benedict C, Hendrickson L, Strand Å (2007) Genome-wide gene expression analysis reveals a critical role for CRYPTOCHROME1 in the response of Arabidopsis to high irradiance. Plant Physiol 144(3):1391–1406
Knapp AK, Carter GA (1998) Variability in leaf optical properties among 26 species from a broad range of habitats. Am J Bot 85(7):940–946
Koltai H (2011) Strigolactones are regulators of root development. New Phytol 190(3):545–549
Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S, Shealtiel H, Bhattacharya C, Eliahu E, Resnick N, Barg R, Kapulnik Y (2009) Strigolactones’ effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J Plant Growth Regul 29(2):129–136. https://doi.org/10.1007/s00344-009-9122-7
Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Curr Protocols Food Analyt Chem 1(1):F4.3.1-F4.3.8
Lichtenthaler HK, Buschmann C, Doll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res 2(2):115–141. https://doi.org/10.1007/BF00028752
Ling F, Su Q, Jiang H, Cui J, He X, Wu Z, Zhang Z, Liu J, Zhao Y (2020) Effects of strigolactone on photosynthetic and physiological characteristics in salt-stressed rice seedlings. Sci Rep 10(1):1–8
Lojkova L, Vranová V, Formánek P, Drápelová I, Brtnicky M, Datta R (2020) Enantiomers of carbohydrates and their role in ecosystem interactions: a review. Symmetry 12(3):470
Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178(4):863–874. https://doi.org/10.1111/j.1469-8137.2008.02406.x
Lopez-Raez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Verstappen F, Bugg TDH, Thompson AJ, Ruyter-Spira C, Bouwmeester H (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187(2):343–354. https://doi.org/10.1111/j.1469-8137.2010.03291.x
López-Ráez JA (2016) How drought and salinity affect arbuscular mycorrhizal symbiosis and strigolactone biosynthesis? Planta 243(6):1375–1385
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(12):550. https://doi.org/10.1186/s13059-014-0550-8
Lu H, Zhang G, Wan T, Lu Y (2011) Influences of light and oxygen conditions on photosynthetic bacteria macromolecule degradation: different metabolic pathways. Bioresour Technol 102(20):9503–9508. https://doi.org/10.1016/j.biortech.2011.07.114
Mashiguchi K, Sasaki E, Shimada Y, Nagae M, Ueno K, Nakano T, Yoneyama K, Suzuki Y, Asami T (2009) Feedback-regulation of strigolactone biosynthetic genes and strigolactone-regulated genes in Arabidopsis. Biosci Biotechnol Biochem 73(11):2460–2465
Mattila H, Mishra KB, Kuusisto I, Mishra A, Novotna K, Sebela D, Tyystjarvi E (2020) Effects of low temperature on photoinhibition and singlet oxygen production in four natural accessions of Arabidopsis. Planta 252(2):19. https://doi.org/10.1007/s00425-020-03423-0
Mayzlish-Gati E, LekKala SP, Resnick N, Wininger S, Bhattacharya C, Lemcoff JH, Kapulnik Y, Koltai H (2010) Strigolactones are positive regulators of light-harvesting genes in tomato. J Exp Bot 61(11):3129–3136. https://doi.org/10.1093/jxb/erq138
Mishra A, Heyer AG, Mishra KB (2014) Chlorophyll fluorescence emission can screen cold tolerance of cold acclimated Arabidopsis thaliana accessions. Plant Methods 10:38. https://doi.org/10.1186/1746-4811-10-38
Mishra KB, Mishra A, Novotna K, Rapantova B, Hodanova P, Urban O, Klem K (2016) Chlorophyll a fluorescence, under half of the adaptive growth-irradiance, for high-throughput sensing of leaf-water deficit in Arabidopsis thaliana accessions. Plant Methods 12:46. https://doi.org/10.1186/s13007-016-0145-3
Mishra KB, Mishra A, Kubasek J, Urban O, HeyerGovindjee AG (2019) Low temperature induced modulation of photosynthetic induction in non-acclimated and cold-acclimated Arabidopsis thaliana: chlorophyll a fluorescence and gas-exchange measurements. Photosynth Res 139(1–3):123–143. https://doi.org/10.1007/s11120-018-0588-7
Nedbal L, Soukupová J, Kaftan D, Whitmarsh J, Trtílek M (2000) Kinetic imaging of chlorophyll fluorescence using modulated light. Photosynth Res 66(1–2):3–12. https://doi.org/10.1023/a:1010729821876
Nedbal L, Cerveny J, Rascher U, Schmidt H (2007) E-photosynthesis: a comprehensive modeling approach to understand chlorophyll fluorescence transients and other complex dynamic features of photosynthesis in fluctuating light. Photosynth Res 93(1–3):223–234. https://doi.org/10.1007/s11120-007-9178-9
Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108(21):8897–8902. https://doi.org/10.1073/pnas.1100987108
Omoarelojie LO, Kulkarni MG, Finnie JF, Van Staden J (2019) Strigolactones and their crosstalk with other phytohormones. Ann Bot 124(5):749–767. https://doi.org/10.1093/aob/mcz100
Omoarelojie LO, Kulkarni MG, Finnie JF, Pospíšil T, Strnad M, Van Staden J (2020) Synthetic strigolactone (rac-GR24) alleviates the adverse effects of heat stress on seed germination and photosystem II function in lupine seedlings. Plant Physiol Biochem 155:965–979
Omoarelojie LO, Kulkarni MG, Finnie JF, Van Staden J (2021) Strigolactone analog (rac-GR24) enhances chilling tolerance in mung bean seedlings. S Afr J Bot 140:173–181
Pandey P, Irulappan V, Bagavathiannan MV, Senthil-Kumar M (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00537
Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, Koltai H (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202(4):1184–1196. https://doi.org/10.1111/nph.12744
Pang Z, Chong J, Zhou G, de Lima Morais DA, Chang L, Barrette M, Gauthier C, Jacques PE, Li S, Xia J (2021) MetaboAnalyst 5.0: narrowing the gap between raw spectra and functional insights. Nucleic Acids Res 49(W1):W388–W396. https://doi.org/10.1093/nar/gkab382
Pereira A (2016) Plant Abiotic Stress Challenges from the Changing Environment. Front Plant Sci 7:1123. https://doi.org/10.3389/fpls.2016.01123
Qu B, Qin Y, Bai Y (2020) From signaling to function: how strigolactones regulate plant development. Sci China Life Sci 63(11):1768–1770. https://doi.org/10.1007/s11427-020-1802-y
Ren C-G, Kong C-C, Xie Z-H (2018) Role of abscisic acid in strigolactone-induced salt stress tolerance in arbuscular mycorrhizal Sesbania cannabina seedlings. BMC Plant Biol 18(1):1–10
Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2(3):198–206
Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009) Soluble sugars–metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4(5):388–393. https://doi.org/10.4161/psb.4.5.8294
Rossel JB, Wilson IW, Pogson BJ (2002) Global changes in gene expression in response to high light in Arabidopsis. Plant Physiol 130(3):1109–1120
Ruban AV (2015) Evolution under the sun: optimizing light harvesting in photosynthesis. J Exp Bot 66(1):7–23. https://doi.org/10.1093/jxb/eru400
Ruban AV (2016) Nonphotochemical chlorophyll fluorescence quenching: mechanism and effectiveness in protecting plants from photodamage. Plant Physiol 170(4):1903–1916. https://doi.org/10.1104/pp.15.01935
Ruiz-Lozano JM, Aroca R, Zamarreno AM, Molina S, Andreo-Jimenez B, Porcel R, Garcia-Mina JM, Ruyter-Spira C, Lopez-Raez JA (2016) Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ 39(2):441–452. https://doi.org/10.1111/pce.12631
Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155(2):721–734
Sami F, Yusuf M, Faizan M, Faraz A, Hayat S (2016) Role of sugars under abiotic stress. Plant Physiol Biochem 109:54–61. https://doi.org/10.1016/j.plaphy.2016.09.005
Schöttler MA, Tóth SZ (2014) Photosynthetic complex stoichiometry dynamics in higher plants: environmental acclimation and photosynthetic flux control. Front Plant Sci 5:188
Sedaghat M, Emam Y, Mokhtassi-Bidgoli A, Hazrati S, Lovisolo C, Visentin I, Cardinale F, Tahmasebi-Sarvestani Z (2021) The potential of the synthetic strigolactone analogue gr24 for the maintenance of photosynthesis and yield in winter wheat under drought: investigations on the mechanisms of action and delivery modes. Plants (Basel) 10(6):1223. https://doi.org/10.3390/plants10061223
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(1):e1001474. https://doi.org/10.1371/journal.pbio.1001474
Smith D, Barkman TJ, dePamphilis CW (2001) Hemiparasitism. Elsevier, pp 70–78
Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (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(3):746–759
Solymosi K, Schoefs B (2010) Etioplast and etio-chloroplast formation under natural conditions: the dark side of chlorophyll biosynthesis in angiosperms. Photosynth Res 105(2):143–166. https://doi.org/10.1007/s11120-010-9568-2
Stirnberg P, van De Sande K, Leyser HO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129(5):1131–1141
Szabados L, Savoure A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97. https://doi.org/10.1016/j.tplants.2009.11.009
Tan M, Li G, Chen X, Xing L, Ma J, Zhang D, Ge H, Han M, Sha G, An N (2019) Role of cytokinin, strigolactone, and auxin export on outgrowth of axillary buds in apple. Front Plant Sci 10:616. https://doi.org/10.3389/fpls.2019.00616
Toh S, Holbrook-Smith D, Stokes ME, Tsuchiya Y, McCourt P (2014) Detection of parasitic plant suicide germination compounds using a high-throughput Arabidopsis HTL/KAI2 strigolactone perception system. Chem Biol 21(8):988–998. https://doi.org/10.1016/j.chembiol.2014.07.005
Torres-Vera R, García JM, Pozo MJ, López-Ráez JA (2014) Do strigolactones contribute to plant defence? Mol Plant Pathol 15(2):211–216. https://doi.org/10.1111/mpp.12074
Tsuchiya Y, Vidaurre D, Toh S, Hanada A, Nambara E, Kamiya Y, Yamaguchi S, McCourt P (2010) A small-molecule screen identifies new functions for the plant hormone strigolactone. Nat Chem Biol 6(10):741–749
Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455(7210):195–200
Van Ha C, Leyva-González MA, Osakabe Y, Tran UT, Nishiyama R, Watanabe Y, Tanaka M, Seki M, Yamaguchi S, Van Dong N (2014) Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc Natl Acad Sci 111(2):851–856
Visentin I, Pagliarani C, Deva E, Caracci A, Turečková V, Novák O, Lovisolo C, Schubert A, Cardinale F (2020) A novel strigolactone-miR156 module controls stomatal behaviour during drought recovery. Plant, Cell Environ 43(7):1613–1624
Walters RG (2005) Towards an understanding of photosynthetic acclimation. J Exp Bot 56(411):435–447
Waters MT, Scaffidi A, Moulin SL, Sun YK, Flematti GR, Smith SM (2015) A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 Functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. Plant Cell 27(7):1925–1944. https://doi.org/10.1105/tpc.15.00146
White ARF, Mendez JA, Khosla A, Nelson DC (2022) Rapid analysis of strigolactone receptor activity in a Nicotiana benthamiana dwarf14 mutant. Plant Direct 6(3):e389. https://doi.org/10.1002/pld3.389
Wu G, Ma L, Sayre RT, Lee CH (2020) Identification of the optimal light harvesting antenna size for high-light stress mitigation in plants. Front Plant Sci 11:505. https://doi.org/10.3389/fpls.2020.00505
Yadav A, Singh D, Lingwan M, Yadukrishnan P, Masakapalli SK, Datta S (2020) Light signaling and UV-B-mediated plant growth regulation. J Integr Plant Biol 62(9):1270–1292. https://doi.org/10.1111/jipb.12932
Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240(2):399–408
Yin R, Skvortsova MY, Loubéry S, Ulm R (2016) COP1 is required for UV-B–induced nuclear accumulation of the UVR8 photoreceptor. Proc Natl Acad Sci 113(30):E4415–E4422
Yoneyama K, Brewer PB (2021) Strigolactones, how are they synthesized to regulate plant growth and development? Curr Opin Plant Biol 63:102072. https://doi.org/10.1016/j.pbi.2021.102072
Zhang Y, Van Dijk AD, Scaffidi A, Flematti GR, Hofmann M, Charnikhova T, Verstappen F, Hepworth J, Van Der Krol S, Leyser O (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10(12):1028–1033
Zhang X, Zhang L, Sun Y, Zheng S, Wang J, Zhang T (2020) Hydrogen peroxide is involved in strigolactone induced low temperature stress tolerance in rape seedlings (Brassica rapa L.). Plant Physiol Biochem 157:402–415
Zhao X, Du Q, Zhao Y, Wang H, Li Y, Wang X, Yu H (2016) Effects of different potassium stress on leaf photosynthesis and chlorophyll fluorescence in maize (Zea mays L.) at seedling stage. Agric Sci 7:44–53
Zheng J, Hong K, Zeng L, Wang L, Kang S, Qu M, Dai J, Zou L, Zhu L, Tang Z, Meng X, Wang B, Hu J, Zeng D, Zhao Y, Cui P, Wang Q, Qian Q, Wang Y, Li J, Xiong G (2020) Karrikin signaling acts parallel to and additively with strigolactone signaling to regulate rice mesocotyl elongation in darkness. Plant Cell 32(9):2780–2805. https://doi.org/10.1105/tpc.20.00123
Zhuang L, Ge Y, Wang J, Yu J, Yang Z, Huang B (2019) Gibberellic acid inhibition of tillering in tall fescue involving crosstalks with cytokinins and transcriptional regulation of genes controlling axillary bud outgrowth. Plant Sci 287:110168. https://doi.org/10.1016/j.plantsci.2019.110168
Acknowledgements
We thank Prof. Jiří Friml and Ms Michelle Gallei for helpful discussion. This project received funding from the European Union’s Horizon 2020 research and innovation program under the Marie Skłodowska-Curie Actions and is co-financed by the South Moravian Region under grant agreement No. 665860 (Si. Si). Additional funding was obtained as Start-up Research Grant (SRG/2021/001707) from DST-SERB, Government of India (Si. Si). The project was funded by The Ministry of Education, Youth and Sports/MEYS of the Czech Republic under the project CEITEC 2020 (LQ1601) (TN, TRM). PK was supported by the European Regional Development Fund, the Project Phytophthora Research Center Reg. No. CZ.02.1.01/0.0/0.0/15_003/0000453. KBM thanks support from the Ministry of Education, Youth and Sports of CR project “SustES—Adaptation strategies for sustainable ecosystem services and food security under adverse environmental conditions” (CZ.02.1.01/0.0/0.0/16_019/0000797). Access to computing and storage facilities owned by parties and projects contributing to the national grid infrastructure, MetaCentrum, provided under the program “Projects of Large Infrastructure for Research, Development, and Innovations” (LM2010005) is greatly appreciated. This article reflects only the authors’ views, and the EU is not responsible for any use that may be made of the information it contains.
Author information
Authors and Affiliations
Contributions
ST, TRM, and SS contributed to conceptualization and data curation; ST and TRM contributed to formal analysis and methodology; SS and TN contributed to funding acquisition; SS contributed to supervision; ST, TRM, PK, MB, KBH, VB, and HS contributed to investigation; ST, TRM, SS, PK, MB, KBH, TN, and SS contributed to writing—review and editing. All authors have read and agreed to the published version of the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
On behalf of all authors, the corresponding author states that there is no conflict of interest.
Additional information
Handling Editor: Tariq Aftab.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Thula, S., Moturu, T.R., Salava, H. et al. Strigolactones Stimulate High Light Stress Adaptation by Modulating Photosynthesis Rate in Arabidopsis. J Plant Growth Regul 42, 4818–4833 (2023). https://doi.org/10.1007/s00344-022-10764-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-022-10764-5