Priming thermotolerance: unlocking heat resilience for climate-smart crops
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
40439313
PubMed Central
PMC12121387
DOI
10.1098/rstb.2024.0234
Knihovny.cz E-zdroje
- Klíčová slova
- crop resilience, global warming, heat stress, priming, thermomemory, thermotolerance,
- MeSH
- klimatické změny * MeSH
- reakce na tepelný šok MeSH
- termotolerance * MeSH
- vysoká teplota MeSH
- zemědělské plodiny * fyziologie genetika MeSH
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Rising temperatures and heat waves pose a substantial threat to crop productivity by disrupting essential physiological and reproductive processes. While plants have a genetically inherited capacity to acclimate to high temperatures, the thermotolerance capacity of many crops remains limited. This limitation leads to yield losses, which are further intensified by the increasing intensity of climate change. In this review, we explore how thermopriming enhances plant resilience by preparing plants for future heat stress (HS) events and summarize the mechanisms underlying the memory of HS (thermomemory) in different plant tissues and organs. We also discuss recent advances in priming agents, including chemical, microbial and physiological interventions, and their application strategies to extend thermotolerance beyond inherent genetic capacity. Additionally, this review examines how integrating priming strategies with genetic improvements, such as breeding and genome editing for thermotolerance traits, provides a holistic solution to mitigate the impact of climate change on agriculture. By combining these approaches, we propose a framework for developing climate-resilient crops and ensuring global food security in the face of escalating environmental challenges.This article is part of the theme issue 'Crops under stress: can we mitigate the impacts of climate change on agriculture and launch the 'Resilience Revolution'?'.
Cyprus University of Technology Limassol Cyprus
Institute of Biochemistry and Biology University of Potsdam Potsdam Germany
Institute of Biology Leiden Leiden University Leiden The Netherlands
Institute of Experimental Botany Czech Academy of Sciences Prague Czech Republic
Institute of Molecular Biosciences Goethe Universitat Frankfurt am Main Frankfurt am Main Germany
Institute of Plant Sciences Agricultural Research Organization Rishon LeZion Israel
Institute of Plant Sciences Paris Saclay Universite Paris Saclay Gif sur Yvette France
Molecular Cell and Systems Biology University of Glasgow Glasgow UK
Zobrazit více v PubMed
IPCC . 2023. Climate change 2023 synthesis report. p. 13. AR6 Synthesis Report. IPCC. See https://www.ipcc.ch/report/ar6/syr/.
Schmidt M, Felsche E. 2024. The effect of climate change on crop yield anomaly in Europe. Clim. Resil. Sustain. 3, e61. (10.1002/cli2.61) DOI
Wahid A, Gelani S, Ashraf M, Foolad M. 2007. Heat tolerance in plants: an overview. Environ. Exp. Bot. 61, 199–223. (10.1016/j.envexpbot.2007.05.011) DOI
Bokszczanin KL, Fragkostefanakis S, Consortium SI, Fragkostefanakis S. 2013. Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front. Plant Sci. 4, 1–20. (10.3389/fpls.2013.00315) PubMed DOI PMC
Wahid A, Close TJ. 2007. Expression of dehydrins under heat stress and their relationship with water relations of sugarcane leaves. Biol. Plant. 51, 104–109. (10.1007/s10535-007-0021-0) DOI
Zhang J, Li XM, Lin HX, Chong K. 2019. Crop improvement through temperature resilience. Annu. Rev. Plant Biol. 70, 753–780. (10.1146/annurev-arplant-050718-100016) PubMed DOI
Ding Y, Yang S. 2022. Surviving and thriving: how plants perceive and respond to temperature stress. Dev. Cell 57, 947–958. (10.1016/j.devcel.2022.03.010) PubMed DOI
Guihur A, Rebeaud ME, Goloubinoff P. 2022. How do plants feel the heat and survive? Trends Biochem. Sci. 47, 824–838. (10.1016/j.tibs.2022.05.004) PubMed DOI
Kerbler SM, Wigge PA. 2023. Temperature sensing in plants. Annu. Rev. Plant Biol. 74, 341–366. (10.1146/annurev-arplant-102820-102235) PubMed DOI
Yeh C-H, Kaplinsky NJ, Hu C, Charng Y-y. 2012. Some like it hot, some like it warm: phenotyping to explore thermotolerance diversity. Plant Sci. 195, 10–23. (10.1016/j.plantsci.2012.06.004) PubMed DOI PMC
Bakery A, Vraggalas S, Shalha B, Chauhan H, Benhamed M, Fragkostefanakis S. 2024. Heat stress transcription factors as the central molecular rheostat to optimize plant survival and recovery from heat stress. New Phytol. 244, 51–64. (10.1111/nph.20017) PubMed DOI
Mishra SK, Tripp J, Winkelhaus S, Tschiersch B, Theres K, Nover L, Scharf KD. 2002. In the complex family of heat stress transcription factors, HsfA1 has a unique role as master regulator of thermotolerance in tomato. Genes Dev. 16, 1555–1567. (10.1101/gad.228802) PubMed DOI PMC
Liu HC, Liao HT, Charng YY. 2011. The role of class A1 heat shock factors (HSFA1s) in response to heat and other stresses in Arabidopsis. Plant Cell Environ. 34, 738–751. (10.1111/j.1365-3040.2011.02278.x) PubMed DOI
Larkindale J, Hall JD, Knight MR, Vierling E. 2005. Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol. 138, 882–897. (10.1104/pp.105.062257) PubMed DOI PMC
Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S. 2006. Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J. 48, 535–547. (10.1111/j.1365-313x.2006.02889.x) PubMed DOI
Ikeda M, Mitsuda N, Ohme-Takagi M. 2011. Arabidopsis HsfB1 and HsfB2b act as repressors of the expression of heat-inducible Hsfs but positively regulate the acquired thermotolerance. Plant Physiol. 157, 1243–1254. (10.1104/pp.111.179036) PubMed DOI PMC
Fragkostefanakis S, et al. . 2016. HsfA2 controls the activity of developmentally and stress-regulated heat stress protection mechanisms in tomato male reproductive tissues. Plant Physiol. 170, 2461–2477. (10.1104/pp.15.01913) PubMed DOI PMC
Mesihovic A, et al. . 2022. HsfA7 coordinates the transition from mild to strong heat stress response by controlling the activity of the master regulator HsfA1a in tomato. Cell Rep. 38, 110224. (10.1016/j.celrep.2021.110224) PubMed DOI
Hilker M, et al. . 2016. Priming and memory of stress responses in organisms lacking a nervous system. Biol. Rev. Camb. Phil. Soc. 49, 1118–1133. (10.1111/brv.12215) PubMed DOI
Lämke J, Brzezinka K, Altmann S, Bäurle I. 2016. A hit‐and‐run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J. 35, 162–175. (10.15252/embj.201592593) PubMed DOI PMC
Bäurle I. 2016. Plant heat adaptation: priming in response to heat stress. F1000Res. 5, 694. (10.12688/f1000research.7526.1) PubMed DOI PMC
Balazadeh S. 2022. A ‘hot’ cocktail: the multiple layers of thermomemory in plants. Curr. Opin. Plant Biol. 65, 102147. (10.1016/j.pbi.2021.102147) PubMed DOI
Liu H, Able AJ, Able JA. 2022. Priming crops for the future: rewiring stress memory. Trends Plant Sci. 27, 699–716. (10.1016/j.tplants.2021.11.015) PubMed DOI
Charng YY, Mitra S, Yu SJ. 2023. Maintenance of abiotic stress memory in plants: lessons learned from heat acclimation. Plant Cell 35, 187–200. (10.1093/plcell/koac313) PubMed DOI PMC
Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I. 2014. Arabidopsis miR156 regulates tolerance to recurring environmental stress through SPL transcription factors. Plant Cell 26, 1792–1807. (10.1105/tpc.114.123851) PubMed DOI PMC
Liu HC, Lämke J, Lin SY, Hung MJ, Liu KM, Charng YY, Bäurle I. 2018. Distinct heat shock factors and chromatin modifications mediate the organ‐autonomous transcriptional memory of heat stress. Plant J. 95, 401–413. (10.1111/tpj.13958) PubMed DOI
Friedrich T, Faivre L, Bäurle I, Schubert D. 2019. Chromatin-based mechanisms of temperature memory in plants. Plant Cell Environ. 42, 762–770. (10.1111/pce.13373) PubMed DOI
Huang Y, et al. . 2023. HSFA1a modulates plant heat stress responses and alters the 3D chromatin organization of enhancer-promoter interactions. Nat. Commun. 14, 469. (10.1038/s41467-023-36227-3) PubMed DOI PMC
Brzezinka K, et al. . 2016. Arabidopsis FORGETTER1 mediates stress-induced chromatin memory through nucleosome remodeling. eLife 5, 1–23. (10.7554/eLife.17061) PubMed DOI PMC
Pratx L, Crawford T, Bäurle I. 2024. Mechanisms of heat stress-induced transcriptional memory. Curr. Opin. Plant Biol. 81, 102590. (10.1016/j.pbi.2024.102590) PubMed DOI
Ding Y, Ndamukong I, Xu Z, Lapko H, Fromm M, Avramova Z. 2012. ATX1-generated H3K4me3 is required for efficient elongation of transcription, not initiation, at ATX1-regulated genes. PLoS Genet. 8, e1003111. (10.1371/journal.pgen.1003111) PubMed DOI PMC
Shang L, et al. . 2021. A mutation in a C2H2-type zinc finger transcription factor contributed to the transition toward self-pollination in cultivated tomato. Plant Cell 33, 3293–3308. (10.1093/plcell/koab201) PubMed DOI PMC
Yamaguchi N, Ito T. 2021. JMJ histone demethylases balance H3K27me3 and H3K4me3 levels at the HSP21 locus during heat acclimation in Arabidopsis. Biomolecules 11, 852. (10.3390/biom11060852) PubMed DOI PMC
Yamaguchi N, et al. . 2021. H3K27me3 demethylases alter HSP22 and HSP17.6C expression in response to recurring heat in Arabidopsis. Nat. Commun. 12, 3480. (10.1038/s41467-021-23766-w) PubMed DOI PMC
Friedrich T, et al. . 2021. Heteromeric HSFA2/HSFA3 complexes drive transcriptional memory after heat stress in Arabidopsis. Nat. Commun. 12, 3426. (10.1038/s41467-021-23786-6) PubMed DOI PMC
Wang H, Fan Z, Shliaha PV, Miele M, Hendrickson RC, Jiang X, Helin K. 2023. H3K4me3 regulates RNA polymerase II promoter-proximal pause-release. Nature 615, 339–348. (10.1038/s41586-023-05780-8) PubMed DOI PMC
Crawford T, Siebler L, Sulkowska A, Nowack B, Jiang L, Pan Y, Lämke J, Kappel C, Bäurle I. 2024. The Mediator kinase module enhances polymerase activity to regulate transcriptional memory after heat stress in Arabidopsis. EMBO J. 43, 437–461. (10.1038/s44318-023-00024-x) PubMed DOI PMC
Oberkofler V, Bäurle I. 2022. Inducible epigenome editing probes for the role of histone H3K4 methylation in Arabidopsis heat stress memory. Plant Physiol. 189, 703–714. (10.1093/plphys/kiac113) PubMed DOI PMC
Charng YY, Liu HC, Liu NY, Chi WT, Wang CN, Chang SH, Wang TT. 2006. A heat-inducible transcription factor, HsfA2, is required for extension of acquired thermotolerance in Arabidopsis. Plant Physiol. 143, 251–262. (10.1104/pp.106.091322) PubMed DOI PMC
Molinier J, Ries G, Zipfel C, Hohn B. 2006. Transgeneration memory of stress in plants. Nature 442, 1046–1049. (10.1038/nature05022) PubMed DOI
Suter L, Widmer A. 2013. Environmental heat and salt stress induce transgenerational phenotypic changes in Arabidopsis thaliana. PLoS One 8, e60364. (10.1371/journal.pone.0060364) PubMed DOI PMC
Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J. 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472, 115–120. (10.1038/nature09861) PubMed DOI
Matsunaga W, Kobayashi A, Kato A, Ito H. 2012. The effects of heat induction and the siRNA biogenesis pathway on the transgenerational transposition of ONSEN, a copia-like retrotransposon in Arabidopsis thaliana. Plant Cell Physiol. 53, 824–833. (10.1093/pcp/pcr179) PubMed DOI
Sharma M, Kumar P, Verma V, Sharma R, Bhargava B, Irfan M. 2022. Understanding plant stress memory response for abiotic stress resilience: molecular insights and prospects. Plant Physiol. Biochem. 179, 10–24. (10.1016/j.plaphy.2022.03.004) PubMed DOI
Singh PK, Miller G, Faigenboim A, Lieberman-lazarovich M. 2021. The tomato ddm1b mutant shows decreased sensitivity to heat stress accompanied by transcriptional alterations. Genes (Basel) 12, 1337. (10.3390/genes12091337) PubMed DOI PMC
Ling Y, et al. . 2018. Thermopriming triggers splicing memory in Arabidopsis. J. Exp. Bot. 69, 2659–2675. (10.1093/jxb/ery062) PubMed DOI PMC
Rosenkranz RRE, et al. . 2024. A plant-specific clade of serine/arginine-rich proteins regulates RNA splicing homeostasis and thermotolerance in tomato. Nucleic Acids Res. 52, 11466–11480. (10.1093/nar/gkae730) PubMed DOI PMC
Ling Y, Mahfouz MM, Zhou S. 2021. Pre-mRNA alternative splicing as a modulator for heat stress response in plants. Trends Plant Sci. 26, 1153–1170. (10.1016/j.tplants.2021.07.008) PubMed DOI
Rosenkranz RRE, Ullrich S, Löchli K, Simm S, Fragkostefanakis S. 2022. Relevance and regulation of alternative splicing in plant heat stress response: current understanding and future directions. Front. Plant Sci. 13, 1–16. (10.3389/fpls.2022.911277) PubMed DOI PMC
Van Nguyen AH, et al. . 2014. Loss of Arabidopsis 5′–3′ exoribonuclease AtXRN4 function enhances heat stress tolerance of plants subjected to severe heat stress. Plant Cell Physiol. 56, 1762–1772. (10.1093/pcp/pcv096) PubMed DOI
Serrano N, Ling Y, Bahieldin A, Mahfouz MM. 2019. Thermopriming reprograms metabolic homeostasis to confer heat tolerance. Sci. Rep. 9, 1–14. (10.1038/s41598-018-36484-z) PubMed DOI PMC
Olas JJ, Apelt F, Annunziata MG, John S, Richard SI, Gupta S, Kragler F, Balazadeh S, Mueller-Roeber B. 2021. Primary carbohydrate metabolism genes participate in heat-stress memory at the shoot apical meristem of Arabidopsis thaliana. Mol. Plant 14, 1508–1524. (10.1016/j.molp.2021.05.024) PubMed DOI
Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi‐Shinozaki K, Shinozaki K. 2002. Important roles of drought‐ and cold‐inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 29, 417–426. (10.1046/j.0960-7412.2001.01227.x) PubMed DOI
ElSayed AI, Rafudeen MS, Golldack D. 2014. Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol. 16, 1–8. (10.1111/plb.12053) PubMed DOI
Song C, Chung WS, Lim CO. 2016. Overexpression of heat shock factor gene HsfA3 increases galactinol levels and oxidative stress tolerance in Arabidopsis. Mol. Cells 39, 477–483. (10.14348/molcells.2016.0027) PubMed DOI PMC
Fan Y, et al. . 2018. Heat priming during early reproductive stages enhances thermo-tolerance to post-anthesis heat stress via improving photosynthesis and plant productivity in winter wheat (Triticum aestivum L.). Front. Plant Sci. 9, 805. (10.3389/fpls.2018.00805) PubMed DOI PMC
Wang X, Cai J, Liu F, Jin M, Yu H, Jiang D, Wollenweber B, Dai T, Cao W. 2012. Pre-anthesis high temperature acclimation alleviates the negative effects of post-anthesis heat stress on stem stored carbohydrates remobilization and grain starch accumulation in wheat. J. Cereal Sci. 55, 331–336. (10.1016/j.jcs.2012.01.004) DOI
Hasanuzzaman M, Bhuyan MHM, Zulfiqar F, Raza A, Mohsin S, Mahmud J, Fujita M, Fotopoulos V. 2020. Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9, 681. (10.3390/antiox9080681) PubMed DOI PMC
Wang X, Cai J, Jiang D, Liu F, Dai T, Cao W. 2011. Pre-anthesis high-temperature acclimation alleviates damage to the flag leaf caused by post-anthesis heat stress in wheat. J. Plant Physiol. 168, 585–593. (10.1016/j.jplph.2010.09.016) PubMed DOI
Delamare J, Brunel-Muguet S, Morvan-Bertrand A, Cantat O, Firmin S, Trinsoutrot-Gattin I, Le Franc L, Personeni E. 2023. Thermopriming effects on root morphological traits and root exudation during the reproductive phase in two species with contrasting strategies: Brassica napus (L.) and Camelina sativa (L.) Crantz. Environ. Exp. Bot. 210, 105318. (10.1016/j.envexpbot.2023.105318) DOI
Ru C, Hu X, Chen D, Wang W, Song T. 2022. Heat and drought priming induce tolerance to subsequent heat and drought stress by regulating leaf photosynthesis, root morphology, and antioxidant defense in maize seedlings. Environ. Exp. Bot. 202, 105010. (10.1016/j.envexpbot.2022.105010) DOI
He J, Tan C, Qin L. 2022. Root-zone heat priming effects on maximum quantum efficiency of PSII, productivity, root morphology and nutritional quality of two aeroponically grown leafy greens in a tropical greenhouse. Plants 11, 1684. (10.3390/plants11131684) PubMed DOI PMC
John S, et al. . 2023. The transcription factor HSFA7b controls thermomemory at the shoot apical meristem by regulating ethylene biosynthesis and signaling in Arabidopsis. Plant Commun. 5, 100743. (10.1016/j.xplc.2023.100743) PubMed DOI PMC
Peng S, Huang J, Sheehy JE, Laza RC, Visperas RM, Zhong X, Centeno GS, Khush GS, Cassman KG. 2004. Rice yields decline with higher night temperature from global warming. Proc. Natl Acad. Sci. USA 101, 9971–9975. (10.1073/pnas.0403720101) PubMed DOI PMC
Liu JX, Liao DQ, Oane R, Estenor L, Yang XE, Li ZC, Bennett J. 2006. Genetic variation in the sensitivity of anther dehiscence to drought stress in rice. Field Crop. Res. 97, 87–100. (10.1016/j.fcr.2005.08.019) DOI
Barnabás B, Jäger K, Fehér A. 2008. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31, 11–38. (10.1111/j.1365-3040.2007.01727.x) PubMed DOI
Su Z, Ma X, Guo H, Sukiran NL, Guo B, Assmann SM, Ma H. 2013. Flower development under drought stress: morphological and transcriptomic analyses reveal acute responses and long-term acclimation in Arabidopsis. Plant Cell 25, 3785–3807. (10.1105/tpc.113.115428) PubMed DOI PMC
Lohani N, Singh MB, Bhalla PL. 2020. High temperature susceptibility of sexual reproduction in crop plants. J. Exp. Bot. 71, 555–568. (10.1093/jxb/erz426) PubMed DOI
Mareri L, Faleri C, Aloisi I, Parrotta L, Del Duca S, Cai G. 2021. Insights into the mechanisms of heat priming and thermotolerance in tobacco pollen. Int. J. Mol. Sci. 22, 8535. (10.3390/ijms22168535) PubMed DOI PMC
Fragkostefanakis S, Mesihovic A, Hu Y, Schleiff E. 2016. Unfolded protein response in pollen development and heat stress tolerance. Plant Reprod. 29, 81–91. (10.1007/s00497-016-0276-8) PubMed DOI
Chaturvedi P, Wiese AJ, Ghatak A, Záveská Drábková L, Weckwerth W, Honys D. 2021. Heat stress response mechanisms in pollen development. New Phytol. 231, 571–585. (10.1111/nph.17380) PubMed DOI PMC
Giorno F, Wolters-Arts M, Grillo S, Scharf KD, Vriezen WH, Mariani C. 2010. Developmental and heat stress-regulated expression of HsfA2 and small heat shock proteins in tomato anthers. J. Exp. Bot. 61, 453–462. (10.1093/jxb/erp316) PubMed DOI PMC
Rezaul IMd, Baohua F, Tingting C, Weimeng F, Caixia Z, Longxing T, Guanfu F. 2019. Abscisic acid prevents pollen abortion under high‐temperature stress by mediating sugar metabolism in rice spikelets. Physiol. Plant. 165, 644–663. (10.1111/ppl.12759) PubMed DOI
Sakata T, et al. . 2010. Auxins reverse plant male sterility caused by high temperatures. Proc. Natl Acad. Sci. USA 107, 8569–8574. (10.1073/pnas.1000869107) PubMed DOI PMC
Firon N, Pressman E, Meir S, Khoury R, Altahan L. 2012. Ethylene is involved in maintaining tomato (Solanum lycopersicum) pollen quality under heat-stress conditions. AoB Plants 2012, pls024. (10.1093/aobpla/pls024) PubMed DOI PMC
Endo M, Tsuchiya T, Hamada K, Kawamura S, Yano K, Ohshima M, Higashitani A, Watanabe M, Kawagishi-Kobayashi M. 2009. High temperatures cause male sterility in rice plants with transcriptional alterations during pollen development. Plant Cell Physiol. 50, 1911–1922. (10.1093/pcp/pcp135) PubMed DOI
Müller F, Xu J, Kristensen L, Wolters-Arts M, de Groot PFM, Jansma SY, Mariani C, Park S, Rieu I. 2016. High-temperature-induced defects in tomato (Solanum lycopersicum) anther and pollen development are associated with reduced expression of B-class floral patterning genes. PLoS One 11, e0167614. (10.1371/journal.pone.0167614) PubMed DOI PMC
Sharma M, Laxmi A. 2016. Jasmonates: emerging players in controlling temperature stress tolerance. Front. Plant Sci. 6, 1129. (10.3389/fpls.2015.01129) PubMed DOI PMC
Balfagón D, Sengupta S, Gómez-Cadenas A, Fritschi FB, Azad RK, Mittler R, Zandalinas SI. 2019. Jasmonic acid is required for plant acclimation to a combination of high light and heat stress. Plant Physiol. 181, 1668–1682. (10.1104/pp.19.00956) PubMed DOI PMC
del Río LA. 2015. ROS and RNS in plant physiology: an overview. J. Exp. Bot. 66, 2827–2837. (10.1093/jxb/erv099) PubMed DOI
Rutley N, Miller G, Wang F, Harper JF, Miller G, Lieberman-Lazarovich M. 2021. Enhanced reproductive thermotolerance of the tomato high pigment 2 mutant is associated with increased accumulation of flavonols in pollen. Front. Plant Sci. 12, 672368. (10.3389/fpls.2021.672368) PubMed DOI PMC
Dong Q, Wallrad L, Almutairi BO, Kudla J. 2022. Ca2+ signaling in plant responses to abiotic stresses. J. Integr. Plant Biol. 64, 287–300. (10.1111/jipb.13228) PubMed DOI
Xu T, Niu J, Jiang Z. 2022. Sensing mechanisms: calcium signaling mediated abiotic stress in plants. Front. Plant Sci. 13, 925863. (10.3389/fpls.2022.925863) PubMed DOI PMC
Lenzoni G, Knight MR. 2019. Increases in absolute temperature stimulate free calcium concentration elevations in the chloroplast. Plant Cell Physiol. 60, 538–548. (10.1093/pcp/pcy227) PubMed DOI
Pollastri S, Sukiran NA, Jacobs BCIC, Knight MR. 2021. Chloroplast calcium signalling regulates thermomemory. J. Plant Physiol. 264, 153470. (10.1016/j.jplph.2021.153470) PubMed DOI
Sedaghatmehr M, Thirumalaikumar VP, Kamranfar I, Marmagne A, Masclaux-Daubresse C, Balazadeh S. 2019. A regulatory role of autophagy for resetting the memory of heat stress in plants. Plant Cell Environ. 42, 1054–1064. (10.1111/pce.13426) PubMed DOI
Sedaghatmehr M, Balazadeh S. 2024. Autophagy: a key player in the recovery of plants from heat stress. J. Exp. Bot. 75, 2246–2255. (10.1093/jxb/erae018) PubMed DOI PMC
Zhou L, Asad M, Guan X, Pan G, Zhang Y, Cheng F. 2024. Rice myo‐inositol‐3‐phosphate synthase 2 (RINO2) alleviates heat injury‐induced impairment in pollen germination and tube growth by modulating Ca2+ signaling and actin filament cytoskeleton. Plant J. 119, 861–878. (10.1111/tpj.16802) PubMed DOI
Antoniou C, Savvides A, Christou A, Fotopoulos V. 2016. Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Curr. Opin. Plant Biol. 33, 101–107. (10.1016/j.pbi.2016.06.020) PubMed DOI
Fancy NN, Bahlmann AK, Loake GJ. 2017. Nitric oxide function in plant abiotic stress. Plant Cell Environ. 40, 462–472. (10.1111/pce.12707) PubMed DOI
Hossain MA, Li ZG, Hoque TS, Burritt DJ, Fujita M, Munné-Bosch S. 2018. Heat or cold priming-induced cross-tolerance to abiotic stresses in plants: key regulators and possible mechanisms. Protoplasma 255, 399–412. (10.1007/s00709-017-1150-8) PubMed DOI
Peláez-Vico MÁ, Fichman Y, Zandalinas SI, Foyer CH, Mittler R. 2024. ROS are universal cell-to-cell stress signals. Curr. Opin. Plant Biol. 79, 102540. (10.1016/j.pbi.2024.102540) PubMed DOI
Bi A, et al. . 2021. Stress memory gene FaHSP17.8-CII controls thermotolerance via remodeling PSII and ROS signaling in tall fescue. Plant Physiol. 187, 1163–1176. (10.1093/plphys/kiab205) PubMed DOI PMC
Sharma M, Banday ZZ, Shukla BN, Laxmi A. 2019. Glucose-regulated HLP1 acts as a key molecule in governing thermomemory. Plant Physiol. 180, 1081–1100. (10.1104/pp.18.01371) PubMed DOI PMC
Wang Q, Yu F, Xie Q. 2020. Balancing growth and adaptation to stress: crosstalk between brassinosteroid and abscisic acid signaling. Plant Cell Environ. 43, 2325–2335. (10.1111/pce.13846) PubMed DOI
Bittner A, Cieśla A, Gruden K, Lukan T, Mahmud S, Teige M, Vothknecht UC, Wurzinger B. 2022. Organelles and phytohormones: a network of interactions in plant stress responses. J. Exp. Bot. 73, 7165–7181. (10.1093/jxb/erac384) PubMed DOI PMC
Waadt R, Seller CA, Hsu PK, Takahashi Y, Munemasa S, Schroeder JI. 2022. Plant hormone regulation of abiotic stress responses. Nat. Rev. Mol. Cell Biol. 23, 680–694. (10.1038/s41580-022-00479-6) PubMed DOI PMC
Huang J, Zhao X, Bürger M, Chory J, Wang X. 2023. The role of ethylene in plant temperature stress response. Trends Plant Sci. 28, 808–824. (10.1016/j.tplants.2023.03.001) PubMed DOI
Zebosi B, Vollbrecht E, Best NB. 2024. Brassinosteroid biosynthesis and signaling: conserved and diversified functions of core genes across multiple plant species. Plant Commun. 5, 100982. (10.1016/j.xplc.2024.100982) PubMed DOI PMC
Zhao J, Wang J, Liu J, Zhang P, Kudoyarova G, Liu CJ, Zhang K. 2024. Spatially distributed cytokinins: metabolism, signaling, and transport. Plant Commun. 5, 100936. (10.1016/j.xplc.2024.100936) PubMed DOI PMC
Yao X, et al. . 2022. Brassinosteroids enhance BES1‐required thermomemory in Arabidopsis thaliana. Plant Cell Environ. 45, 3492–3504. (10.1111/pce.14444) PubMed DOI
Albertos P, Dündar G, Schenk P, Carrera S, Cavelius P, Sieberer T, Poppenberger B. 2022. Transcription factor BES1 interacts with HSFA1 to promote heat stress resistance of plants. EMBO J. 41, e108664. (10.15252/embj.2021108664) PubMed DOI PMC
He NY, Chen LS, Sun AZ, Zhao Y, Yin SN, Guo FQ. 2022. A nitric oxide burst at the shoot apex triggers a heat-responsive pathway in Arabidopsis. Nat. Plants 8, 434–450. (10.1038/s41477-022-01135-9) PubMed DOI
Zandalinas SI, Mittler R. 2022. Plant responses to multifactorial stress combination. New Phytol. 234, 1161–1167. (10.1111/nph.18087) PubMed DOI
Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K. 2006. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl Acad. Sci. USA 103, 18822–18827. (10.1073/pnas.0605639103) PubMed DOI PMC
Liu JX, Srivastava R, Che P, Howell SH. 2007. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J. 51, 897–909. (10.1111/j.1365-313x.2007.03195.x) PubMed DOI PMC
Howell SH. 2013. Endoplasmic reticulum stress responses in plants. Annu. Rev. Plant Biol. 64, 477–499. (10.1146/annurev-arplant-050312-120053) PubMed DOI
Huang YC, Niu CY, Yang CR, Jinn TL. 2016. The heat-stress factor HSFA6b connects ABA signaling and ABA-mediated heat responses. Plant Physiol. 172, 1182–1199. (10.1104/pp.16.00860) PubMed DOI PMC
Zang D, Wang J, Zhang X, Liu Z, Wang Y. 2019. Arabidopsis heat shock transcription factor HSFA7b positively mediates salt stress tolerance by binding to an E-box-like motif to regulate gene expression. J. Exp. Bot. 70, 5355–5374. (10.1093/jxb/erz261) PubMed DOI PMC
Mishra SK, et al. . 2024. Heat-stress-responsive HvHSFA2e gene regulates the heat and drought tolerance in barley through modulation of phytohormone and secondary metabolic pathways. Plant Cell Rep. 43, 172. (10.1007/s00299-024-03251-6) PubMed DOI
Zhang X, Cai J, Wollenweber B, Liu F, Dai T, Cao W, Jiang D. 2013. Multiple heat and drought events affect grain yield and accumulations of high molecular weight glutenin subunits and glutenin macropolymers in wheat. J. Cereal Sci. 57, 134–140. (10.1016/j.jcs.2012.10.010) DOI
Zhang X, Wang X, Zhong J, Zhou Q, Wang X, Cai J, Dai T, Cao W, Jiang D. 2016. Drought priming induces thermo-tolerance to post-anthesis high-temperature in offspring of winter wheat. Environ. Exp. Bot. 127, 26–36. (10.1016/j.envexpbot.2016.03.004) DOI
Wan SB, et al. . 2009. Involvement of phospholipase D in the low temperature acclimation-induced thermotolerance in grape berry. Plant Physiol. Biochem. 47, 504–510. (10.1016/j.plaphy.2008.12.010) PubMed DOI
Perrella G, Zioutopoulou A, Headland LR, Kaiserli E. 2020. The impact of light and temperature on chromatin organization and plant adaptation. J. Exp. Bot. 71, 5247–5255. (10.1093/jxb/eraa154) PubMed DOI
Cheng Q, Zeng Y, Huang S, Yang C, Xie Y, Shen WH, Li L. 2024. Phytochrome-interacting factor 7 and relative of early flowering 6 act in shade avoidance memory in Arabidopsis. Nat. Commun. 15, 8032. (10.1038/s41467-024-51834-4) PubMed DOI PMC
Tan W, et al. . 2023. The heat response regulators HSFA1s promote Arabidopsis thermomorphogenesis via stabilizing PIF4 during the day. Sci. Adv. 9, eadh1738. (10.1126/sciadv.adh1738) PubMed DOI PMC
Verma N, Singh D, Mittal L, Banerjee G, Noryang S, Sinha AK. 2024. MPK4-mediated phosphorylation of phytochrome interacting factor4 controls thermosensing by regulating histone variant H2A.Z deposition. Plant Cell 36, 4535–4556. (10.1093/plcell/koae223) PubMed DOI PMC
Xin X, et al. . 2024. Temperature-dependent jumonji demethylase modulates flowering time by targeting H3K36me2/3 in Brassica rapa. Nat. Commun. 15, 5470. (10.1038/s41467-024-49721-z) PubMed DOI PMC
Jung JH, et al. . 2016. Phytochromes function as thermosensors in Arabidopsis. Science 354, 886–889. (10.1126/science.aaf6005) PubMed DOI
Willige BC, et al. . 2021. Phytochrome-interacting factors trigger environmentally responsive chromatin dynamics in plants. Nat. Genet. 53, 955–961. (10.1038/s41588-021-00882-3) PubMed DOI PMC
Kim RJA, Fan D, He J, Kim K, Du J, Chen M. 2024. Photobody formation spatially segregates two opposing phytochrome B signaling actions of PIF5 degradation and stabilization. Nat. Commun. 15, 3519. (10.1038/s41467-024-47790-8) PubMed DOI PMC
Xue M, Zhang H, Zhao F, Zhao T, Li H, Jiang D. 2021. The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis. Mol. Plant 14, 1799–1813. (10.1016/j.molp.2021.07.001) PubMed DOI
Gao J, et al. . 2023. Blue light receptor CRY1 regulates HSFA1d nuclear localization to promote plant thermotolerance. Cell Rep. 42, 113117. (10.1016/j.celrep.2023.113117) PubMed DOI PMC
González Guzmán M, Cellini F, Fotopoulos V, Balestrini R, Arbona V. 2022. New approaches to improve crop tolerance to biotic and abiotic stresses. Physiol. Plant. 174, e13547. (10.1111/ppl.13547) PubMed DOI PMC
Kollist H, Zandalinas SI, Sengupta S, Nuhkat M, Kangasjärvi J, Mittler R. 2019. Rapid responses to abiotic stress: priming the landscape for the signal transduction network. Trends Plant Sci. 24, 25–37. (10.1016/j.tplants.2018.10.003) PubMed DOI
Christou A, Filippou P, Manganaris GA, Fotopoulos V. 2014. Sodium hydrosulfide induces systemic thermotolerance to strawberry plants through transcriptional regulation of heat shock proteins and aquaporin. BMC Plant Biol. 14, 1–11. (10.1186/1471-2229-14-42) PubMed DOI PMC
Li Z, et al. . 2017. The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Front. Plant Sci. 8, 1153. (10.3389/fpls.2017.01153) PubMed DOI PMC
Kata LP, Bhaskaran M, Umarani R. 2014. Influence of priming treatments on stress tolerance during seed germination of rice. Int. J. Agric. Environ. Biotech. 7, 225–232. (10.5958/2230-732X.2014.00238.1) DOI
Matsui A, et al. . 2022. Ethanol induces heat tolerance in plants by stimulating unfolded protein response. Plant Mol. Biol. 110, 131–145. (10.1007/s11103-022-01291-8) PubMed DOI
Yamauchi Y, Kunishima M, Mizutani M, Sugimoto Y. 2015. Reactive short-chain leaf volatiles act as powerful inducers of abiotic stress-related gene expression. Sci. Rep. 5, 8030. (10.1038/srep08030) PubMed DOI PMC
Postiglione AE, et al. . 2024. Flavonols improve tomato pollen thermotolerance during germination and tube elongation by maintaining reactive oxygen species homeostasis. Plant Cell 36, 4511–4534. (10.1093/plcell/koae222) PubMed DOI PMC
Cabral C, Ravnskov S, Tringovska I, Wollenweber B. 2016. Arbuscular mycorrhizal fungi modify nutrient allocation and composition in wheat (Triticum aestivum L.) subjected to heat-stress. Plant Soil 408, 385–399. (10.1007/s11104-016-2942-x) DOI
Anderson M, Habiger J. 2012. Characterization and identification of productivity-associated rhizobacteria in wheat. Appl. Environ. Microbiol. 78, 4434–4446. (10.1128/aem.07466-11) PubMed DOI PMC
Szentpéteri V, Virág E, Mayer Z, Duc NH, Hegedűs G, Posta K. 2024. First peek into the transcriptomic response in heat-stressed tomato inoculated with Septoglomus constrictum. Plants 13, 2266. (10.3390/plants13162266) PubMed DOI PMC
Zulfikar Ali S, Sandhya V, Grover M, Linga VR, Bandi V. 2011. Effect of inoculation with a thermotolerant plant growth promoting Pseudomonas putida strain AKMP7 on growth of wheat (Triticum spp.) under heat stress. J. Plant Interact. 6, 239–246. (10.1080/17429145.2010.545147) DOI
Khan MA, Asaf S, Khan AL, Jan R, Kang SM, Kim KM, Lee IJ. 2020. Thermotolerance effect of plant growth-promoting Bacillus cereus SA1 on soybean during heat stress. BMC Microbiol. 20, 1–14. (10.1186/s12866-020-01822-7) PubMed DOI PMC
Shekhawat K, et al. . 2021. Root endophyte induced plant thermotolerance by constitutive chromatin modification at heat stress memory gene loci. EMBO Rep. 22, 1–15. (10.15252/embr.202051049) PubMed DOI PMC
Orozco-Mosqueda MC, Glick BR, Santoyo G. 2020. ACC deaminase in plant growth-promoting bacteria (PGPB): an efficient mechanism to counter salt stress in crops. Microbiol. Res. 235, 126439. (10.1016/j.micres.2020.126439) PubMed DOI
Mareri L, Cai G. 2022. Plant stress pollen priming for more efficient reproduction in a heating world: what we know, what we need to know. Plant Stress 3, 100060. (10.1016/j.stress.2022.100060) DOI
Wang X, Vignjevic M, Jiang D, Jacobsen S, Wollenweber B. 2014. Improved tolerance to drought stress after anthesis due to priming before anthesis in wheat (Triticum aestivum L.) var. Vinjett. J. Exp. Bot. 65, 6441–6456. (10.1093/jxb/eru362) PubMed DOI PMC
Fang S, Gao K, Hu W, Snider JL, Wang S, Chen B, Zhou Z. 2018. Chemical priming of seed alters cotton floral bud differentiation by inducing changes in hormones, metabolites and gene expression. Plant Physiol. Biochem. 130, 633–640. (10.1016/j.plaphy.2018.08.010) PubMed DOI
Zubler AV, Yoon JY. 2020. Proximal methods for plant stress detection using optical sensors and machine learning. Biosensors 10, 193. (10.3390/bios10120193) PubMed DOI PMC
Jain M. 2024. Gene regulatory networks in abiotic stress responses via single-cell sequencing and spatial technologies: advances and opportunities. Curr. Opin. Plant Biol. 82, 102662. (10.1016/j.pbi.2024.102662) PubMed DOI
Tian X, et al. . 2020. Heat shock transcription factor A1b regulates heat tolerance in wheat and Arabidopsis through OPR3 and jasmonate signalling pathway. Plant Biotechnol. J. 18, 1109–1111. (10.1111/pbi.13268) PubMed DOI PMC
Wang H, et al. . 2023. Thermosensitive SUMOylation of TaHsfA1 defines a dynamic ON/OFF molecular switch for the heat stress response in wheat. Plant Cell 35, 3889–3910. (10.1093/plcell/koad192) PubMed DOI PMC
Hu Y, et al. . 2020. Natural variation in HsfA2 pre‐mRNA splicing is associated with changes in thermotolerance during tomato domestication. New Phytol. 225, 1297–1310. (10.1111/nph.16221) PubMed DOI
Lin MY, Chai KH, Ko SS, Kuang LY, Lur HS, Charng YY. 2014. A positive feedback loop between HEAT SHOCK PROTEIN101 and HEAT STRESS-ASSOCIATED 32-KD PROTEIN modulates long-term acquired thermotolerance illustrating diverse heat stress responses in rice varieties. Plant Physiol. 164, 2045–2053. (10.1104/pp.113.229609) PubMed DOI PMC
Gohari G, Jiang M, Manganaris GA, Zhou J, Fotopoulos V. 2024. Next generation chemical priming: with a little help from our nanocarrier friends. Trends Plant Sci. 29, 150–166. (10.1016/j.tplants.2023.11.024) PubMed DOI
Antoniou C, Xenofontos R, Chatzimichail G, Christou A, Kashfi K, Fotopoulos V. 2020. Exploring the potential of nitric oxide and hydrogen sulfide (NOSH)-releasing synthetic compounds as novel priming agents against drought stress in Medicago sativa plants. Biomolecules 10, 120. (10.3390/biom10010120) PubMed DOI PMC
Rocha I, Ma Y, Souza-Alonso P, Vosátka M, Freitas H, Oliveira RS. 2019. Seed coating: a tool for delivering beneficial microbes to agricultural crops. Front. Plant Sci. 10, 1357. (10.3389/fpls.2019.01357) PubMed DOI PMC
Nair AU, Prasad D, Bhukya N, Sunkar R, Chavali S. 2022. Molecular basis of priming-induced acquired tolerance to multiple abiotic stresses in plants. J. Exp. Bot. 73, 3355–3371. (10.1093/jxb/erac089) PubMed DOI
Kerchev P, van der Meer T, Sujeeth N, Verlee A, Stevens CV, Van Breusegem F, Gechev T. 2020. Molecular priming as an approach to induce tolerance against abiotic and oxidative stresses in crop plants. Biotechnol. Adv. 40, 107503. (10.1016/j.biotechadv.2019.107503) PubMed DOI
Di Stasio E, Cirillo V, Raimondi G, Giordano M, Esposito M, Maggio A. 2020. Osmo-priming with seaweed extracts enhances yield of salt-stressed tomato plants. Agronomy 10, 1559. (10.3390/agronomy10101559) DOI
Berruto CA, Demirer GS. 2024. Engineering agricultural soil microbiomes and predicting plant phenotypes. Trends Microbiol. 32, 858–873. (10.1016/j.tim.2024.02.003) PubMed DOI