Progress in Salicylic Acid-Dependent Signaling for Growth–Defense Trade-Off
Abstract
:1. Introduction
2. SA Biosynthesis, Perception, and Signaling in Defense and Growth
3. Environmental Conditions Modulate SA Biosynthesis and SA Signaling
3.1. Temperature
3.2. Atmospheric CO2
3.3. Nutrient Status Modulates SA-Dependent Immunity
4. Emerging Roles of Development and Primary Metabolism in Defense
5. Breeding Strategies to Overcome Growth–Defense Trade-Off
6. Conclusions and Perspectives
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Huot, B.; Yao, J.; Montgomery, B.L.; He, S.Y. Growth–Defense Tradeoffs in Plants: A Balancing Act to Optimize Fitness. Mol. Plant 2014, 7, 1267–1287. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Hilleary, R.; Seroka, A.; He, S.Y. Crops of the future: Building a climate-resilient plant immune system. Curr. Opin. Plant Biol. 2021, 60, 101997. [Google Scholar] [CrossRef] [PubMed]
- Prasch, C.M.; Sonnewald, U. Simultaneous Application of Heat, Drought, and Virus to Arabidopsis Plants Reveals Significant Shifts in Signaling Networks. Plant Physiol. 2013, 162, 1849–1866. [Google Scholar] [CrossRef] [PubMed]
- Zhang, H.; Sonnewald, U. Differences and commonalities of plant responses to single and combined stresses. Plant J. 2017, 90, 839–855. [Google Scholar] [CrossRef]
- Rizhsky, L.; Liang, H.; Shuman, J.; Shulaev, V.; Davletova, S.; Mittler, R. When Defense Pathways Collide. The Response of Arabidopsis to a Combination of Drought and Heat Stress. Plant Physiol. 2004, 134, 1683–1696. [Google Scholar] [CrossRef]
- Rasmussen, S.; Barah, P.; Suarez-Rodriguez, M.C.; Bressendorff, S.; Friis, P.; Costantino, P.; Bones, A.M.; Nielsen, H.B.; Mundy, J. Transcriptome Responses to Combinations of Stresses in Arabidopsis. Plant Physiol. 2013, 161, 1783–1794. [Google Scholar] [CrossRef]
- Ding, P.; Ding, Y. Stories of Salicylic Acid: A Plant Defense Hormone. Trends Plant Sci. 2020, 25, 549–565. [Google Scholar] [CrossRef]
- Peng, Y.; Yang, J.; Li, X.; Zhang, Y. Salicylic Acid: Biosynthesis and Signaling. Annu. Rev. Plant Biol. 2021, 72, 761–791. [Google Scholar] [CrossRef]
- Zhang, L.; Zhang, F.; Melotto, M.; Yao, J.; He, S.Y. Jasmonate signaling and manipulation by pathogens and insects. J. Exp. Bot. 2017, 68, 1371–1385. [Google Scholar] [CrossRef]
- Rekhter, D.; Lüdke, D.; Ding, Y.; Feussner, K.; Zienkiewicz, K.; Lipka, V.; Wiermer, M.; Zhang, Y.; Feussner, I. Isochorismate-derived biosynthesis of the plant stress hormone salicylic acid. Science 2019, 365, 498. [Google Scholar] [CrossRef]
- Yamasaki, K.; Motomura, Y.; Yagi, Y.; Nomura, H.; Kikuchi, S.; Nakai, M.; Shiina, T. Chloroplast envelope localization of EDS5, an essential factor for salicylic acid biosynthesis in Arabidopsis thaliana. Plant Signal. Behav. 2013, 8, e23603. [Google Scholar] [CrossRef] [PubMed]
- Serrano, M.; Wang, B.; Aryal, B.; Garcion, C.; Abou-Mansour, E.; Heck, S.; Geisler, M.; Mauch, F.; Nawrath, C.; Métraux, J.-P. Export of Salicylic Acid from the Chloroplast Requires the Multidrug and Toxin Extrusion-Like Transporter EDS5. Plant Physiol. 2013, 162, 1815–1821. [Google Scholar] [CrossRef] [PubMed]
- Torrens-Spence, M.P.; Bobokalonova, A.; Carballo, V.; Glinkerman, C.M.; Pluskal, T.; Shen, A.; Weng, J.-K. PBS3 and EPS1 Complete Salicylic Acid Biosynthesis from Isochorismate in Arabidopsis. Mol. Plant 2019, 12, 1577–1586. [Google Scholar] [CrossRef] [PubMed]
- Huang, J.; Gu, M.; Lai, Z.; Fan, B.; Shi, K.; Zhou, Y.-H.; Yu, J.-Q.; Chen, Z. Functional Analysis of the Arabidopsis PAL Gene Family in Plant Growth, Development, and Response to Environmental Stress. Plant Physiol. 2010, 153, 1526–1538. [Google Scholar] [CrossRef]
- Ding, Y.; Sun, T.; Ao, K.; Peng, Y.; Zhang, Y.; Li, X.; Zhang, Y. Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity. Cell 2018, 173, 1454–1467. [Google Scholar] [CrossRef] [PubMed]
- Wu, Y.; Zhang, D.; Chu, J.Y.; Boyle, P.; Wang, Y.; Brindle, I.D.; De Luca, V.; Després, C. The Arabidopsis NPR1 Protein Is a Receptor for the Plant Defense Hormone Salicylic Acid. Cell Rep. 2012, 1, 639–647. [Google Scholar] [CrossRef]
- Cao, H.; Glazebrook, J.; Clarke, J.D.; Volko, S.; Dong, X. The Arabidopsis NPR1 Gene That Controls Systemic Acquired Resistance Encodes a Novel Protein Containing Ankyrin Repeats. Cell 1997, 88, 57–63. [Google Scholar] [CrossRef]
- Rochon, A.; Boyle, P.; Wignes, T.; Fobert, P.R.; Després, C. The Coactivator Function of Arabidopsis NPR1 Requires the Core of Its BTB/POZ Domain and the Oxidation of C-Terminal Cysteines. Plant Cell 2006, 18, 3670–3685. [Google Scholar] [CrossRef]
- Rivas-San Vicente, M.; Plasencia, J. Salicylic acid beyond defence: Its role in plant growth and development. J. Exp. Bot. 2011, 62, 3321–3338. [Google Scholar] [CrossRef]
- Gutiérrez-Coronado, M.A.; Trejo-López, C.; Larqué-Saavedra, A. Effects of salicylic acid on the growth of roots and shoots in soybean. Plant Physiol. Biochem. 1998, 36, 563–565. [Google Scholar] [CrossRef]
- Shakirova, F.M.; Sakhabutdinova, A.R.; Bezrukova, M.V.; Fatkhutdinova, R.A.; Fatkhutdinova, D.R. Changes in the hormonal status of wheat seedlings induced by salicylic acid and salinity. Plant Sci. 2003, 164, 317–322. [Google Scholar] [CrossRef]
- Gunes, A.; Inal, A.; Alpaslan, M.; Eraslan, F.; Bagci, E.G.; Cicek, N. Salicylic acid induced changes on some physiological parameters symptomatic for oxidative stress and mineral nutrition in maize (Zea mays L.) grown under salinity. J. Plant Physiol. 2007, 164, 728–736. [Google Scholar] [CrossRef] [PubMed]
- Kovácik, J.; Grúz, J.; Backor, M.; Strnad, M.; Repcák, M. Salicylic acid-induced changes to growth and phenolic metabolism in Matricaria chamomilla plants. Plant Cell Rep. 2009, 28, 135–143. [Google Scholar] [CrossRef] [PubMed]
- van Wersch, R.; Li, X.; Zhang, Y. Mighty Dwarfs: Arabidopsis Autoimmune Mutants and Their Usages in Genetic Dissection of Plant Immunity. Front. Plant Sci. 2016, 7, 1717. [Google Scholar] [CrossRef] [PubMed]
- Abreu, M.E.; Munné-Bosch, S. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J. Exp. Bot. 2009, 60, 1261–1271. [Google Scholar] [CrossRef]
- Samuel, G. Some Experiments On Inoculating Methods With Plant Viruses, And On Local Lesions. Ann. Appl. Biol. 1931, 18, 494–507. [Google Scholar] [CrossRef]
- Dropkin, V.H. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne: Reversal by temperature. Phytopathology 1969, 59, 1632–1637. [Google Scholar]
- Kim, Y.; Park, S.; Gilmour, S.J.; Thomashow, M.F. Roles of CAMTA transcription factors and salicylic acid in configuring the low-temperature transcriptome and freezing tolerance of Arabidopsis. Plant J. 2013, 75, 364–376. [Google Scholar] [CrossRef]
- Wu, Z.; Han, S.; Zhou, H.; Tuang, Z.K.; Wang, Y.; Jin, Y.; Shi, H.; Yang, W. Cold stress activates disease resistance in Arabidopsis thaliana through a salicylic acid dependent pathway. Plant Cell Environ. 2019, 42, 2645–2663. [Google Scholar] [CrossRef]
- Li, Z.; Liu, H.M.; Ding, Z.H.; Yan, J.P.; Yu, H.Y.; Pan, R.H.; Hu, J.; Guan, Y.J.; Hua, J. Low Temperature Enhances Plant Immunity via Salicylic Acid Pathway Genes That Are Repressed by Ethylene. Plant Physiol. 2020, 182, 626–639. [Google Scholar] [CrossRef]
- Whitham, S.; McCormick, S.; Baker, B. The N gene of tobacco confers resistance to tobacco mosaic virus in transgenic tomato. Proc. Natl. Acad. Sci. USA 1996, 93, 8776–8781. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Anfoka, G.; Moshe, A.; Fridman, L.; Amrani, L.; Rotem, O.; Kolot, M.; Zeidan, M.; Czosnek, H.; Gorovits, R. Tomato yellow leaf curl virus infection mitigates the heat stress response of plants grown at high temperatures. Sci. Rep. 2016, 6, 19715. [Google Scholar] [CrossRef] [PubMed]
- Makarova, S.; Makhotenko, A.; Spechenkova, N.; Love, A.J.; Kalinina, N.O.; Taliansky, M. Interactive Responses of Potato (Solanum tuberosum L.) Plants to Heat Stress and Infection With Potato Virus Y. Front. Microbiol. 2018, 9, 2582. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Bao, Z.; Zhu, Y.; Hua, J. Analysis of Temperature Modulation of Plant Defense Against Biotrophic Microbes. Mol. Plant Microbe Interact. 2009, 22, 498–506. [Google Scholar] [CrossRef]
- Zhu, Y.; Qian, W.; Hua, J. Temperature Modulates Plant Defense Responses through NB-LRR Proteins. PLoS Pathog. 2010, 6, e1000844. [Google Scholar] [CrossRef]
- Noctor, G.; Mhamdi, A. Climate Change, CO2, and Defense: The Metabolic, Redox, and Signaling Perspectives. Trends Plant Sci. 2017, 22, 857–870. [Google Scholar] [CrossRef]
- Niu, Y.; Ahammed, G.J.; Tang, C.; Guo, L.; Yu, J. Physiological and Transcriptome Responses to Combinations of Elevated CO2 and Magnesium in Arabidopsis thaliana. PLoS ONE 2016, 11, e0149301. [Google Scholar] [CrossRef]
- Kane, K.; Dahal, K.P.; Badawi, M.A.; Houde, M.; Hüner, N.P.A.; Sarhan, F. Long-Term Growth Under Elevated CO2 Suppresses Biotic Stress Genes in Non-Acclimated, But Not Cold-Acclimated Winter Wheat. Plant Cell Physiol. 2013, 54, 1751–1768. [Google Scholar] [CrossRef]
- Williams, A.; Petriacq, P.; Schwarzenbacher, R.E.; Beerling, D.J.; Ton, J. Mechanisms of glacial-to-future atmospheric CO2 effects on plant immunity. New Phytol. 2018, 218, 752–761. [Google Scholar] [CrossRef]
- Mhamdi, A.; Noctor, G. High CO2 Primes Plant Biotic Stress Defences through Redox-Linked Pathways. Plant Physiol. 2016, 172, 929–942. [Google Scholar] [CrossRef]
- Zhang, S.; Li, X.; Sun, Z.; Shao, S.; Hu, L.; Ye, M.; Zhou, Y.; Xia, X.; Yu, J.; Shi, K. Antagonism between phytohormone signalling underlies the variation in disease susceptibility of tomato plants under elevated CO2. J. Exp. Bot. 2015, 66, 1951–1963. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vaughan, M.M.; Huffaker, A.; Schmelz, E.A.; Dafoe, N.J.; Christensen, S.; Sims, J.; Martins, V.F.; Swerbilow, J.A.Y.; Romero, M.; Alborn, H.T.; et al. Effects of elevated [CO2] on maize defence against mycotoxigenic Fusarium verticillioides. Plant Cell Environ. 2014, 37, 2691–2706. [Google Scholar] [CrossRef]
- Váry, Z.; Mullins, E.; McElwain, J.C.; Doohan, F.M. The severity of wheat diseases increases when plants and pathogens are acclimatized to elevated carbon dioxide. Glob. Chang. Biol. 2015, 21, 2661–2669. [Google Scholar] [CrossRef] [PubMed]
- Zhou, Y.L.; Van Leeuwen, S.K.; Pieterse, C.M.J.; Bakker, P.; Van Wees, S.C.M. Effect of atmospheric CO2 on plant defense against leaf and root pathogens of Arabidopsis. Eur. J. Plant Pathol. 2019, 154, 31–42. [Google Scholar] [CrossRef]
- Eastburn, D.M.; Degennaro, M.M.; Delucia, E.H.; Dermody, O.; McElrone, A.J. Elevated atmospheric carbon dioxide and ozone alter soybean diseases at SoyFACE. Glob. Change Biol. 2010, 16, 320–330. [Google Scholar] [CrossRef]
- Eastburn, D.M.; McElrone, A.J.; Bilgin, D.D. Influence of atmospheric and climatic change on plant–pathogen interactions. Plant Pathol. 2011, 60, 54–69. [Google Scholar] [CrossRef]
- Galbraith, E.D.; Eggleston, S. A lower limit to atmospheric CO2 concentrations over the past 800,000 years. Nat. Geosci. 2017, 10, 295–298. [Google Scholar] [CrossRef]
- Temme, A.A.; Liu, J.C.; Cornwell, W.K.; Cornelissen, J.H.C.; Aerts, R. Winners always win: Growth of a wide range of plant species from low to future high CO2. Ecol. Evol. 2015, 5, 4949–4961. [Google Scholar] [CrossRef]
- Li, Y.; Xu, J.; Haq, N.U.; Zhang, H.; Zhu, X.-G. Was low CO2 a driving force of C4 evolution: Arabidopsis responses to long-term low CO2 stress. J. Exp. Bot. 2014, 65, 3657–3667. [Google Scholar] [CrossRef]
- Sørhagen, K.; Laxa, M.; Peterhänsel, C.; Reumann, S. The emerging role of photorespiration and non-photorespiratory peroxisomal metabolism in pathogen defence. Plant Biol. 2013, 15, 723–736. [Google Scholar] [CrossRef]
- Chaouch, S.; Queval, G.; Vanderauwera, S.; Mhamdi, A.; Vandorpe, M.; Langlois-Meurinne, M.; Van Breusegem, F.; Saindrenan, P.; Noctor, G. Peroxisomal Hydrogen Peroxide Is Coupled to Biotic Defense Responses by ISOCHORISMATE SYNTHASE1 in a Daylength-Related Manner. Plant Physiol. 2010, 153, 1692–1705. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chaouch, S.; Queval, G.; Noctor, G. AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant J. 2012, 69, 613–627. [Google Scholar] [CrossRef] [PubMed]
- Drake, B.G.; Gonzàlez-Meler, M.A.; Long, S.P. More efficient plants: A Consequence of Rising Atmospheric CO2? Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997, 48, 609–639. [Google Scholar] [CrossRef] [PubMed]
- Williams, A.; Pétriacq, P.; Beerling, D.J.; Cotton, T.E.A.; Ton, J. Impacts of Atmospheric CO2 and Soil Nutritional Value on Plant Responses to Rhizosphere Colonization by Soil Bacteria. Front. Plant Sci. 2018, 9, 1493. [Google Scholar] [CrossRef] [PubMed]
- Mur, L.A.J.; Simpson, C.; Kumari, A.; Gupta, A.K.; Gupta, K.J. Moving nitrogen to the centre of plant defence against pathogens. Ann. Bot. 2017, 119, 703–709. [Google Scholar] [CrossRef] [PubMed]
- Chan, C.; Liao, Y.-Y.; Chiou, T.-J. The Impact of Phosphorus on Plant Immunity. Plant Cell Physiol. 2021, 62, 582–589. [Google Scholar] [CrossRef]
- Masclaux-Daubresse, C.; Daniel-Vedele, F.; Dechorgnat, J.; Chardon, F.; Gaufichon, L.; Suzuki, A. Nitrogen uptake, assimilation and remobilization in plants: Challenges for sustainable and productive agriculture. Ann. Bot. 2010, 105, 1141–1157. [Google Scholar] [CrossRef]
- Mus, F.; Crook Matthew, B.; Garcia, K.; Garcia Costas, A.; Geddes Barney, A.; Kouri Evangelia, D.; Paramasivan, P.; Ryu, M.-H.; Oldroyd Giles, E.D.; Poole Philip, S.; et al. Symbiotic Nitrogen Fixation and the Challenges to Its Extension to Nonlegumes. Appl. Environ. Microbiol. 2016, 82, 3698–3710. [Google Scholar] [CrossRef]
- Hoffland, E.; Jeger, M.J.; van Beusichem, M.L. Effect of nitrogen supply rate on disease resistance in tomato depends on the pathogen. Plant Soil 2000, 218, 239–247. [Google Scholar] [CrossRef]
- Huang, H.; Nguyen Thi Thu, T.; He, X.; Gravot, A.; Bernillon, S.; Ballini, E.; Morel, J.B. Increase of fungal pathogenicity and role of plant glutamine in nitrogen-induced susceptibility (NIS) to rice blast. Front. Plant Sci. 2017, 8, 265. [Google Scholar] [CrossRef]
- Ballini, E.; Nguyen, T.T.T.; Morel, J.B. Diversity and genetics of Nitrogen-Induced Susceptibility to the blast fungus in rice and wheat. Rice 2013, 6, 1–13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoffland, E.; van Beusichem, M.L.; Jeger, M.J. Nitrogen availability and susceptibility of tomato leaves to Botrytis cinerea. Plant Soil 1999, 210, 263–272. [Google Scholar] [CrossRef]
- Solomon, P.S.; Oliver, R.P. The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta 2001, 213, 241–249. [Google Scholar] [CrossRef] [PubMed]
- Pageau, K.; Reisdorf-Cren, M.; Morot-Gaudry, J.F.; Masclaux-Daubresse, C. The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. J. Exp. Bot. 2006, 57, 547–557. [Google Scholar] [CrossRef] [PubMed]
- Tavernier, V.; Cadiou, S.; Pageau, K.; Lauge, R.; Reisdorf-Cren, M.; Langin, T.; Masclaux-Daubresse, C. The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. J. Exp. Bot. 2007, 58, 3351–3360. [Google Scholar] [CrossRef]
- López-Berges, M.S.; Rispail, N.; Prados-Rosales, R.C.; Di Pietro, A. A Nitrogen Response Pathway Regulates Virulence Functions in Fusarium oxysporum via the Protein Kinase TOR and the bZIP Protein MeaB. Plant Cell 2010, 22, 2459–2475. [Google Scholar] [CrossRef]
- Morcillo, R.J.L.; Singh, S.K.; He, D.; An, G.; Vílchez, J.I.; Tang, K.; Yuan, F.; Sun, Y.; Shao, C.; Zhang, S.; et al. Rhizobacterium-derived diacetyl modulates plant immunity in a phosphate-dependent manner. EMBO J. 2020, 39, e102602. [Google Scholar] [CrossRef]
- Khan, G.A.; Vogiatzaki, E.; Glauser, G.; Poirier, Y. Phosphate Deficiency Induces the Jasmonate Pathway and Enhances Resistance to Insect Herbivory. Plant Physiol. 2016, 171, 632–644. [Google Scholar] [CrossRef]
- Luo, X.; Li, Z.; Xiao, S.; Ye, Z.; Nie, X.; Zhang, X.; Kong, J.; Zhu, L. Phosphate deficiency enhances cotton resistance to Verticillium dahliae through activating jasmonic acid biosynthesis and phenylpropanoid pathway. Plant Sci. 2021, 302, 110724. [Google Scholar] [CrossRef]
- Hewezi, T.; Piya, S.; Qi, M.; Balasubramaniam, M.; Rice, J.H.; Baum, T.J. Arabidopsis miR827 mediates post-transcriptional gene silencing of its ubiquitin E3 ligase target gene in the syncytium of the cyst nematode Heterodera schachtii to enhance susceptibility. Plant J. 2016, 88, 179–192. [Google Scholar] [CrossRef]
- Yaeno, T.; Iba, K. BAH1/NLA, a RING-Type Ubiquitin E3 Ligase, Regulates the Accumulation of Salicylic Acid and Immune Responses to Pseudomonas syringae DC3000. Plant Physiol. 2008, 148, 1032–1041. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Castrillo, G.; Teixeira, P.J.P.L.; Paredes, S.H.; Law, T.F.; de Lorenzo, L.; Feltcher, M.E.; Finkel, O.M.; Breakfield, N.W.; Mieczkowski, P.; Jones, C.D.; et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature 2017, 543, 513–518. [Google Scholar] [CrossRef] [PubMed]
- Campos-Soriano, L.; Bundo, M.; Bach-Pages, M.; Chiang, S.F.; Chiou, T.J.; San Segundo, B. Phosphate excess increases susceptibility to pathogen infection in rice. Mol. Plant Pathol. 2020, 21, 555–570. [Google Scholar] [CrossRef]
- Val-Torregrosa, B.; Bundó, M.; Mallavarapu, M.D.; Chiou, T.-J.; Flors, V.; San Segundo, B. Loss-of-function of NITROGEN LIMITATION ADAPTATION confers disease resistance in Arabidopsis by modulating hormone signaling and camalexin content. Plant Sci. 2022, 323, 111374. [Google Scholar] [CrossRef] [PubMed]
- Val-Torregrosa, B.; Bundó, M.; Martín-Cardoso, H.; Bach-Pages, M.; Chiou, T.-J.; Flors, V.; Segundo, B.S. Phosphate-induced resistance to pathogen infection in Arabidopsis. Plant J. 2022, 110, 452–469. [Google Scholar] [CrossRef] [PubMed]
- Hassler, S.; Lemke, L.; Jung, B.; Möhlmann, T.; Krüger, F.; Schumacher, K.; Espen, L.; Martinoia, E.; Neuhaus, H.E. Lack of the Golgi phosphate transporter PHT4;6 causes strong developmental defects, constitutively activated disease resistance mechanisms and altered intracellular phosphate compartmentation in Arabidopsis. Plant J. 2012, 72, 732–744. [Google Scholar] [CrossRef] [PubMed]
- Wang, G.-Y.; Shi, J.-L.; Ng, G.; Battle, S.L.; Zhang, C.; Lu, H. Circadian Clock-Regulated Phosphate Transporter PHT4;1 Plays an Important Role in Arabidopsis Defense. Mol. Plant 2011, 4, 516–526. [Google Scholar] [CrossRef]
- Dong, Z.; Li, W.; Liu, J.; Li, L.H.; Pan, S.J.; Liu, S.J.; Gao, J.; Liu, L.; Liu, X.L.; Wang, G.L.; et al. The Rice Phosphate Transporter Protein OsPT8 Regulates Disease Resistance and Plant Growth. Sci. Rep. 2019, 9, 5408. [Google Scholar] [CrossRef]
- Zhang, J.; Lu, Z.; Pan, Y.; Ren, T.; Cong, R.; Lu, J.; Li, X. Potassium deficiency aggravates yield loss in rice by restricting the translocation of non-structural carbohydrates under Sarocladium oryzae infection condition. Physiol. Plant. 2019, 167, 352–364. [Google Scholar] [CrossRef]
- Yermiyahu, U.; Israeli, L.; David, D.R.; Faingold, I.; Elad, Y. Higher potassium concentration in shoots reduces gray mold in sweet basil. Phytopathology 2015, 105, 1059–1068. [Google Scholar] [CrossRef]
- Zhang, Z.; Chao, M.; Wang, S.; Bu, J.; Tang, J.; Li, F.; Wang, Q.; Zhang, B. Proteome quantification of cotton xylem sap suggests the mechanisms of potassium-deficiency-induced changes in plant resistance to environmental stresses. Sci. Rep. 2016, 6, 1–15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kus, J.V.; Zaton, K.; Sarkar, R.; Cameron, R.K. Age-Related Resistance in Arabidopsis Is a Developmentally Regulated Defense Response to Pseudomonas syringae. Plant Cell 2002, 14, 479–490. [Google Scholar] [CrossRef] [PubMed]
- Zeier, J. Age-dependent variations of local and systemic defence responses in Arabidopsis leaves towards an avirulent strain of Pseudomonas syringae. Physiol. Mol. Plant Pathol. 2005, 66, 30–39. [Google Scholar] [CrossRef]
- Hensel, L.L.; Grbić, V.; Baumgarten, D.A.; Bleecker, A.B. Developmental and age-related processes that influence the longevity and senescence of photosynthetic tissues in arabidopsis. Plant Cell 1993, 5, 553–564. [Google Scholar] [CrossRef] [PubMed]
- Berens, M.L.; Wolinska, K.W.; Spaepen, S.; Ziegler, J.; Nobori, T.; Nair, A.; Kruler, V.; Winkelmuller, T.M.; Wang, Y.M.; Mine, A.; et al. Balancing trade-offs between biotic and abiotic stress responses through leaf age-dependent variation in stress hormone cross-talk. Proc. Natl. Acad. Sci. USA 2019, 116, 2364–2373. [Google Scholar] [CrossRef]
- Leontovycova, H.; Kalachova, T.; Janda, M. Disrupted actin: A novel player in pathogen attack sensing? New Phytol. 2020, 227, 1605–1609. [Google Scholar] [CrossRef]
- Ke, Y.G.; Yuan, M.; Liu, H.B.; Hui, S.G.; Qin, X.F.; Chen, J.; Zhang, Q.L.; Li, X.H.; Xiao, J.H.; Zhang, Q.F.; et al. The versatile functions of OsALDH2B1 provide a genic basis for growth-defense trade-offs in rice. Proc. Natl. Acad. Sci. USA 2020, 117, 3867–3873. [Google Scholar] [CrossRef]
- Durian, G.; Jeschke, V.; Rahikainen, M.; Vuorinen, K.; Gollan, P.J.; Brosche, M.; Salojarvi, J.; Glawischnig, E.; Winter, Z.; Li, S.C.; et al. PROTEIN PHOSPHATASE 2A-B 'gamma Controls Botrytis cinerea Resistance and Developmental Leaf Senescence. Plant Physiol. 2020, 182, 1161–1181. [Google Scholar] [CrossRef]
- Yang, L.; Wang, Z.; Zhang, A.; Bhawal, R.; Li, C.; Zhang, S.; Cheng, L.; Hua, J. Reduction of the canonical function of a glycolytic enzyme enolase triggers immune responses that further affect metabolism and growth in Arabidopsis. Plant Cell 2021, 34, 1745–1767. [Google Scholar] [CrossRef]
- Badet, T.; Leger, O.; Barascud, M.; Voisin, D.; Sadon, P.; Vincent, R.; Le Ru, A.; Balague, C.; Roby, D.; Raffaele, S. Expression polymorphism at the ARPC4 locus links the actin cytoskeleton with quantitative disease resistance to Sclerotinia sclerotiorum in Arabidopsis thaliana. New Phytol. 2019, 222, 480–496. [Google Scholar] [CrossRef]
- Birchler, J.A.; Yao, H.; Chudalayandi, S. Unraveling the genetic basis of hybrid vigor. Proc. Natl. Acad. Sci. USA 2006, 103, 12957–12958. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yang, L.; Li, B.; Zheng, X.-y.; Li, J.; Yang, M.; Dong, X.; He, G.; An, C.; Deng, X.W. Salicylic acid biosynthesis is enhanced and contributes to increased biotrophic pathogen resistance in Arabidopsis hybrids. Nat. Commun. 2015, 6, 7309. [Google Scholar] [CrossRef] [PubMed]
- Yang, L.; Liu, P.T.; Wang, X.C.; Jia, A.L.; Ren, D.Q.; Tang, Y.R.; Tang, Y.Q.; Deng, X.W.; He, G.M. A central circadian oscillator confers defense heterosis in hybrids without growth vigor costs. Nat. Commun. 2021, 12, 1–14. [Google Scholar] [CrossRef] [PubMed]
- Harmer, S.L.; Hogenesch, J.B.; Straume, M.; Chang, H.S.; Han, B.; Zhu, T.; Wang, X.; Kreps, J.A.; Kay, S.A. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 2000, 290, 2110–2113. [Google Scholar] [CrossRef]
- Harmer, S.L.; Kay, S.A. Positive and Negative Factors Confer Phase-Specific Circadian Regulation of Transcription in Arabidopsis. Plant Cell 2005, 17, 1926–1940. [Google Scholar] [CrossRef] [Green Version]
Environmental Conditions | Plant Species | Effect on SA or SA Signaling | Immunity Output | Pathogens/Pests | Ref. |
---|---|---|---|---|---|
Temperature | |||||
Low temperature | Arabidopsis | SA and SAG induced | n/a | n/a | [28] |
Low temperature | Arabidopsis | SA induced | Promote resistance | Pst DC3000 | [29] |
Low temperature | Arabidopsis | SA induced | Promote resistance | Pst DC3000, Cor-, hrcU- | [30] |
High temperature | Arabidopsis | n/a | Promote susceptibility | TMV | [3] |
High temperature | tomato (S. lycopersicum) | n/a | Promote susceptibility | TMV | [31] |
High temperature | tomato (S. lycopersicum) | n/a | Promote susceptibility | TYLCV | [32] |
High temperature | potato (S. tuberosum) | SA signaling more active | Promote susceptibility | PVY | [33] |
in resistant cultivar | |||||
Atmospheric CO2 | |||||
eCO2 | Arabidopsis | SA induced | Promote resistance | P. cucumerina and H. arabidopsidis | [39] |
eCO2 | Arabidopsis | SA induced | Promote resistance | Pst DC3000 and B. cinerea | [40] |
eCO2 | beans (P. vulgaris) | SA induced | n/a | n/a | [40] |
eCO2 | wheat (T. aestivum) | SA induced | n/a | n/a | [40] |
eCO2 | tomato (S. lycopersicum) | SA induced | Promote resistance | TMV, P. syringae, B. cinerea | [41] |
eCO2 | maize (Z. mays) | no change | Promote susceptibility | F. verticillioides | [42] |
eCO2 | wheat (cv. Remus) | n/a | Promote susceptibility | Z. tritici | [43] |
saCO2 | Arabidopsis | SA induced | Promote susceptibility | P. cucumerina | [39] |
saCO2 | Arabidopsis | SA induced | Promote resistance | H. arabidopsidis | [39] |
Nutrient | |||||
High nitrate supply | tomato (S. esculentum) | n/a | Promote susceptibility | Pst DC3000 | [59] |
High nitrate and ammonia supply | rice (O. sativa) | n/a | Promote susceptibility | M.oryzae | [60] |
High nitrate and ammonia supply | rice (O. sativa) | n/a | Promote susceptibility | M.oryzae | [61] |
High nitrate and ammonia supply | wheat (cv. Arche and Récital) | n/a | Promote susceptibility | M.oryzae | [61] |
Ammonium supply | tomato (S. lycopersicum) | n/a | Promote resistance | F. oxysporum | [66] |
Low P supply | Arabidopsis | SA induced | n/a | n/a | [67] |
Low P supply | tomato (S. lycopersicum) | n/a | Promote resistance | S. littoralis and P. brassicae | [68] |
Low P supply | cotton (cv. YZ1) | n/a | Promote resistance | V. dahliae | [69] |
Low P supply, phr1 | Arabidopsis | SA signaling more active | Mutant more resistant | Pst DC3000 | [72] |
pht4;6 | Arabidopsis | SA and SAG induced | Mutant more resistant | Pst DC3000 | [76] |
pht4;1 | Arabidopsis | suppresses SA in acd6-1 | Mutant more resistant | P. syringae pv. maculicola | [77] |
Low K supply | rice (O. sativa) | n/a | Promote susceptibility | S. oryzae | [79] |
Low K supply | cotton (cv. DP99B) | PR-1, PR-5 repressed | n/a | n/a | [81] |
High K supply | sweet basil (O. basilicum) | n/a | Promote resistance | B. cinerea | [80] |
Development and primary metabolism | |||||
Age related resistance (ARR) | Arabidopsis | n/a | sid1, sid2, nahG abolish AAR | P. syringae pv. maculicola | [83] |
los2 (glycolysis) | Arabidopsis | SA induced | Mutant more resistant | Pst DC3000 | [89] |
osaldh2b1 | rice | SA induced | Mutant more resistant | X. oryzae and M. oryzae | [87] |
pp2a-b | Arabidopsis | SA induced | Mutant more resistant | B. cinerea | [88] |
arpc4 | Arabidopsis | SA signaling more active | Mutant more resistant | S. sclerotiorum | [89] |
Breeding strategy | |||||
Hybrids/ heterosis | Arabidopsis | SA induced | Promote resistance | Pst DC3000 | [92] |
Hybrids/ heterosis | Arabidopsis | SA induced | Promote resistance | Pst DC3000 | [93] |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chan, C. Progress in Salicylic Acid-Dependent Signaling for Growth–Defense Trade-Off. Cells 2022, 11, 2985. https://doi.org/10.3390/cells11192985
Chan C. Progress in Salicylic Acid-Dependent Signaling for Growth–Defense Trade-Off. Cells. 2022; 11(19):2985. https://doi.org/10.3390/cells11192985
Chicago/Turabian StyleChan, Ching. 2022. "Progress in Salicylic Acid-Dependent Signaling for Growth–Defense Trade-Off" Cells 11, no. 19: 2985. https://doi.org/10.3390/cells11192985