Strigolactones positively regulate abscisic acid-dependent heat and cold tolerance in tomato

Cheng Chi , Xuechen Xu , Mengqi Wang , Hui Zhang , Pingping Fang , Jie Zhou , Xiaojian Xia , Kai Shi , Yanhong Zhou , Jingquan Yu

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 237

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :237 DOI: 10.1038/s41438-021-00668-y
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Strigolactones positively regulate abscisic acid-dependent heat and cold tolerance in tomato
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Abstract

Strigolactones are carotenoid-derived phytohormones that impact plant growth and development in diverse ways. However, the roles of strigolactones in the responses to temperature stresses are largely unknown. Here, we demonstrated that strigolactone biosynthesis is induced in tomato (Solanum lycopersicum) by heat and cold stresses. Compromised strigolactone biosynthesis or signaling negatively affected heat and cold tolerance, while application of the synthetic strigolactone analog GR245DS enhanced heat and cold tolerance. Strigolactone-mediated heat and cold tolerance was associated with the induction of abscisic acid (ABA), heat shock protein 70 (HSP70) accumulation, C-REPEAT BINDING FACTOR 1 (CBF1) transcription, and antioxidant enzyme activity. Importantly, a deficiency in ABA biosynthesis compromised the GR245DS effects on heat and cold stresses and abolished the GR245DS-induced transcription of HSP70, CBF1, and antioxidant-related genes. These results support that strigolactones positively regulate tomato heat and cold tolerance and that they do so at least partially by the induction of CBFs and HSPs and the antioxidant response in an ABA-dependent manner.

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Cheng Chi, Xuechen Xu, Mengqi Wang, Hui Zhang, Pingping Fang, Jie Zhou, Xiaojian Xia, Kai Shi, Yanhong Zhou, Jingquan Yu. Strigolactones positively regulate abscisic acid-dependent heat and cold tolerance in tomato. Horticulture Research, 2021, 8 (1) : 237 DOI:10.1038/s41438-021-00668-y

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References

[1]

Reddy, A. R., Chaitanya, K. V. & Vivekanandan, M. Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J. Plant Physiol. 161, 1189-1202 (2004).

[2]

Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373-399 (2004).

[3]

Gill, S. S. & Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 48, 909-930 (2010).

[4]

Mittler, R., Vanderauwera, S., Gollery, M. & Van Breusegem, F. Reactive oxygen gene network of plants. Trends Plant Sci. 9, 490-498 (2004).

[5]

Larkindale, J., Hall, J. D., Knight, M. R. & Vierling, E. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882-897 (2005).

[6]

Suzuki, N. & Mittler, R. Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol. Plant. 126, 45-51 (2006).

[7]

Wang, F. et al. Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol. 170, 459-471 (2016).

[8]

Chi, C. et al. Brassinosteroids act as a positive regulator of NBR1-dependent selective autophagy in response to chilling stress in tomato. J. Exp. Bot. 71, 1092-1106 (2020).

[9]

Boston, R. S., Viitanen, P. V. & Vierling, E. Molecular chaperones and protein folding in plants. Plant Mol. Biol. 32, 191-222 (1996).

[10]

Lee, J. H. & Schöfl, F. An Hsp70 antisense gene affects the expression of HSP70/HSC70, the regulation of HSF, and the acquisition of thermotolerance in transgenic Arabidopsis thaliana. Mol. Gen. Genet. 252, 11-19 (1996).

[11]

Li, H. et al. Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ. 37, 2768-2780 (2014).

[12]

Gilmour, S. J. et al. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 16, 433-442 (1998).

[13]

Lee, S. C. & Luan, S. ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ. 35, 53-60 (2012).

[14]

Jiang, M. Y. & Zhang, J. H. Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J. Exp. Bot. 53, 2401-2410 (2002).

[15]

Knight, H., Zarka, D. G., Okamoto, H., Thomashow, M. F. & Knight, M. R. Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 135, 1710-1717 (2004).

[16]

Nir, I. et al. The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. Plant Cell 29, 3186-3197 (2017).

[17]

Liu, X. et al. ζ-Carotene isomerase suppresses tillering in rice through the coordinated biosynthesis of strigolactone and abscisic acid. Mol. Plant 13, 1784-1801 (2020).

[18]

Vogel, J. T. et al. SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. Plant J. 61, 300-311 (2010).

[19]

Kohlen, W. et al. The tomato CAROTENOID CLEAVAGE DIOXYGENASE8 (SlCCD8) regulates rhizosphere signaling, plant architecture and affects reproductive development through strigolactone biosynthesis. New Phytol. 196, 535-547 (2012).

[20]

Zhang, Y. et al. Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat. Chem. Biol. 10, 1028-1033 (2014).

[21]

Yao, R. F. et al. DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536, 469-473 (2016).

[22]

Lv, S. et al. Strigolactone-triggered stomatal closure requires hydrogen peroxide synthesis and nitric oxide production in an abscisic acid-independent manner. New Phytol. 217, 290-304 (2018).

[23]

Agusti, J. et al. Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc. Natl Acad. Sci. USA 108, 20242-20247 (2011).

[24]

Kapulnik, Y. et al. Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233, 209-216 (2011).

[25]

de Jong, M. et al. Auxin and strigolactone signaling are required for modulation of Arabidopsis shoot branching by nitrogen supply. Plant Physiol. 166, 384-395 (2014).

[26]

Ha, C. V. et al. Positive regulatory role of strigolactone in plant responses to drought and salt stress. Proc. Natl Acad. Sci. USA 111, 851-856 (2014).

[27]

Torres-Vera, R., García, J. M., Pozo, M. J. & López-Ráez, J. A. Do strigolactones contributes to plant defence? Mol. Plant Pathol. 15, 211-216 (2014).

[28]

Woo, H. R. et al. ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13, 1779-1790 (2001).

[29]

López-Ráez, J. A. et al. Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol. 178, 863-874 (2008).

[30]

Liu, J. et al. Osmotic stress represses strigolactone biosynthesis in Lotus japonicus roots: exploring the interaction between strigolactones and ABA under abiotic stress. Planta 241, 1435-1451 (2015).

[31]

Visentin, I. et al. Low levels of strigolactones in roots as a component of the systemic signal of drought stress in tomato. New Phytol. 212, 954-963 (2016).

[32]

Visentin, I. et al. A novel strigolactone-miR156 module controls stomatal behaviour during drought recovery. Plant Cell Environ. 43, 1613-1624 (2020).

[33]

Xie, X., Yoneyama, K. & Yoneyama, K. The strigolactone story. Annu. Rev. Phytopathol. 48, 93-117 (2010).

[34]

Kohlen, W. et al. Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol. 155, 974-987 (2011).

[35]

Cooper, J. W. et al. Strigolactones positively regulate chilling tolerance in pea and in Arabidopsis. Plant Cell Environ. 41, 1298-1310 (2018).

[36]

Hu, Q. N., Zhang, S. X. & Huang, B. R. Strigolactones promote leaf elongation in tall fescue through upregulation of cell cycle genes and downregulation of auxin transport genes in tall fescue under different temperature regimes. Int. J. Mol. Sci. 20, 1836 (2019).

[37]

Zhu, J. K. Salt and drought stress signal transduction in plants. Annu. Rev. Plant Biol. 53, 247-273 (2002).

[38]

Li, W. Q. et al. Comparative functional analyses of DWARF14 and KARRIKIN INSENSITIVE 2 in drought adaptation of Arabidopsis thaliana. Plant J. 103, 111-127 (2020).

[39]

Sedaghat, M., Tahmasebi-Sarvestani, Z., Emam, Y. & Mokhtassi-Bidgoli, A. Physiological and antioxidant responses of winter wheat cultivars to strigolactone and salicylic acid in drought. Plant Physiol. Biochem. 119, 59-69 (2017).

[40]

Aroca, R. et al. Arbuscular mycorrhizal symbiosis influences strigolactone production under salinity and alleviates salt stress in lettuce plants. J. Plant Physiol. 170, 47-55 (2013).

[41]

Ruiz-Lozano, J. M. et al. Arbuscular mycorrhizal symbiosis induces strigolactone biosynthesis under drought and improves drought tolerance in lettuce and tomato. Plant Cell Environ. 39, 441-452 (2016).

[42]

Wang, L. et al. Transcriptional regulation of strigolactone signalling in Arabidopsis. Nature 583, 272-281 (2020).

[43]

Haider, I. et al. The interaction of strigolactones with abscisic acid during the drought response in rice. J. Exp. Bot. 69, 2403-2414 (2018).

[44]

Lechat, M. M. et al. PrCYP707A1, an ABA catabolic gene, is a key component of Phelipanche ramosa seed germination in response to the strigolactone analogue GR24. J. Exp. Bot. 63, 5311-5322 (2012).

[45]

Toh, S. et al. Thermoinhibition uncovers a role for strigolactones in Arabidopsis seed germination. Plant Cell Physiol. 53, 107-117 (2012).

[46]

Ferrero, M. et al. Exogenous strigolactone interacts with abscisic acid-mediated accumulation of anthocyanins in grapevine berries. J. Exp. Bot. 69, 2391-2401 (2018).

[47]

De Cuyper, C. et al. Strigolactones, karrikins and beyond. Plant Cell Environ. 40, 1691-1703 (2017).

[48]

Xia, X. J. et al. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150, 801-814 (2009).

[49]

Ma, N. et al. Strigolactones improve plant growth, photosynthesis, and alleviate oxidative stress under salinity in rapeseed (Brassica napus L.) by regulating gene expression. Front. Plant Sci. 8, 1671 (2017).

[50]

Mayzlish-Gati, E. et al. Strigolactones are positive regulators of light-harvesting genes in tomato. J. Exp. Bot. 61, 3129-3136 (2010).

[51]

Burbidge, A. et al. Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J. 17, 427-431 (1999).

[52]

Pan, C. et al. CRISPR/Cas9-mediated efficient and heritable targeted mutagenesis in tomato plants in the first and later generations. Sci. Rep. 6, 24765 (2016).

[53]

Lei, Y. et al. CRISPR-P: a web tool for synthetic single-guide RNA design of CRISPR-system in plants. Mol. Plant 7, 1494-1496 (2014).

[54]

Fillatti, J. J., Kiser, J., Rose, R. & Comai, L. Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat. Biotechnol. 5, 726-730 (1987).

[55]

Challis, R. J., Hepworth, J., Mouchel, C., Waites, R. & Leyser, O. A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol. 161, 1885-1902 (2013).

[56]

Ekengren, S. K., Liu, Y., Schiff, M., Dinesh-Kumar, S. P. & Martin, G. B. Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J. 36, 905-917 (2003).

[57]

Cao, W. H. et al. Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol. 143, 707-719 (2007).

[58]

Ogweno, J. O. et al. Detached leaves of tomato differ in their photosynthetic physiological response to moderate high and low temperature stress. Sci. Hortic. 123, 17-22 (2009).

[59]

Xu, X. C. et al. Strigolactones positively regulate defense against root-knot nematodes in tomato. J. Exp. Bot. 70, 1325-1337 (2019).

[60]

Zhou, J. et al. NBR1-mediated selective autophagy targets insoluble ubiquitinated protein aggregates in plant stress responses. PLoS Genet. 9, e1003196 (2013).

[61]

Willekens, H. et al. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants . EMBO J. 16, 4806-4816 (1997).

[62]

Stewart, R. R. C. & Bewley, J. D. Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol. 65, 245-248 (1980).

[63]

Nakano, Y. & Asada, K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 22, 867-880 (1981).

[64]

Foyer, C. H. & Halliwell, B. The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133, 21-25 (1976).

[65]

Hossain, M. A., Nakano, Y. & Asada, K. Monodehydroascorbate reductase in spinach chloroplasts and its participation in regeneration of ascorbate for scavenging hydrogen peroxide. Plant Cell Physiol. 25, 385-395 (1984).

[66]

Noctor, G., Mhamdi, A. & Foyer, C. H. Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ. 39, 1140-1160 (2016).

[67]

Yin, Y. L. et al. BZR1 transcription factor regulates heat stress tolerance through FERONIA receptor-like kinase-mediated reactive oxygen species signaling in tomato. Plant Cell Physiol. 59, 2239-2254 (2018).

[68]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt Method . Methods 25, 402-408 (2001).

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