Priming Bean Seedlings to Boost Natural Plant Defenses Against Common Bacterial Wilt: Gas Exchange, and Fluorescence Results (Part 2)
PDF

Keywords

Plant priming
Cell hydration
Universal primers
Multifaceted immunity
Common bean wilt disease
Systemic acquired resistance

How to Cite

1.
Ramsey CL, Sandoval VM, Freebury PC, Newman DH, Dooley G, Cseke LJ, Newman SE. Priming Bean Seedlings to Boost Natural Plant Defenses Against Common Bacterial Wilt: Gas Exchange, and Fluorescence Results (Part 2). Glob. J. Agric. Innov. Res. Dev [Internet]. 2023 May 23 [cited 2024 Dec. 23];10:21-5. Available from: https://avantipublisher.com/index.php/gjaird/article/view/1411

Abstract

This greenhouse study evaluated the effects of two chemical primers for kidney bean seedlings against a bacterial wilt (Curtobacterium flaccumfaciens pv. Flaccumfaciens) (CFF). The premise of this study was that the oxidant primers would mimic the signaling properties of radical oxygen species and initiate a cascade of molecular defenses. The factorial study included two levels for the foliar chlorine dioxide treatment, and two levels for the bacterial wilt inoculation treatment, plus two supplemental chemical treatments. The foliage response variables were gas exchange and fluorescence. There was a 36, 154, and 70% reduction in Pn, gs, and E, respectively, at 39 DAT when comparing the inoculated control to the non-inoculated control. The chlorine dioxide primers lowered leaf temperatures and leaf vapor pressure deficit in the CFF wilt inoculated plants. The chlorine dioxide primers improved gas exchange at 39 DAT when compared to the water treatments. Part 1 and 2 of this series conclude that the chlorine dioxide primers can activate a long-term, systemic acquired resistance (SAR) response in kidney bean plants infected with the CFF wilt. The Part 2 article also concludes that the EB treatments caused several inexplicable correlations among the gas exchange responses. A structured water premise was proposed as an explanation for the gas exchange anomalies due to the EB treatments. Intuitively, this study suggests that chlorine dioxide primers can initiate a series of ROS and salicylic acid signals that activate a suite of mechanisms that provide universal, multifaceted plant immunity that is sustained across a crop season.

https://doi.org/10.15377/2409-9813.2023.10.2
PDF

References

Ramsey CL, Sandoval VM, Freebury PC, Newman DH, Dooley G, Cseke LJ, et al. Priming bean seedlings to boost natural plant defenses against common bacterial wilt: salicylic acid responses to chemical inducers (Part 1). Glob J Agric Innov Res Dev. 2023; 10: 1-20. https://doi.org/10.15377/2409-9813.2023.10.1

Zhou J-M, Zhang Y. Plant immunity: danger perception and signaling. Cell 2020; 181: 978-89. https://doi.org/10.1016/j.cell.2020.04.028

Hilker M, Schmülling T. Stress priming, memory, and signalling in plants. Plant Cell Environ. 2019; 42: 753-61. https://doi.org/10.1111/pce.13526

Cooper A, Ton J. Immune priming in plants: from the onset to transgenerational maintenance. Essays Biochem. 2022; 66: 635-46. https://doi.org/10.1042/EBC20210082

Bhar A, Chakraborty A, Roy A. Plant responses to biotic stress: Old memories matter. Plants. 2021; 11(1): 84. https://doi.org/10.3390/plants11010084

Goellner K, Conrath U. Priming: it’s all the world to induced disease resistance. Eur J Plant Path. 2008; 121: 233-42. https://doi.org/10.1007/s10658-007-9251-4

Buswell W, Schwarzenbacher RE, Luna E, Sellwood M, Chen B, Flors V, et al. Chemical priming of immunity without costs to plant growth. New Phytologist. 2018; 218: 1205-16. https://doi.org/10.1111/nph.15062

Andersen E, Ali S, Byamukama E, Yen Y, Nepal M. Disease resistance mechanisms in plants. Genes (Basel). 2018; 9(7): 339. https://doi.org/10.3390/genes9070339

JH D. An overview of plant immunity. J Plant Pathol Microbiol. 2015; 6: 10-4172. https://doi.org/10.4172/2157-7471.1000322

Vallad GE, Goodman RM. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 2004; 44: 1920-34. https://doi.org/10.2135/cropsci2004.1920

Conrath U. Systemic acquired resistance. Plant Signal Behav. 2006; 1: 179-84. https://doi.org/10.4161/psb.1.4.3221

Gozzo F, Faoro F. Systemic acquired resistance (50 years after discovery): moving from the lab to the field. J Agric Food Chem. 2013; 61: 12473-91. https://doi.org/10.1021/jf404156x

Bürger M, Chory J. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe. 2019; 26: 163-72. https://doi.org/10.1016/j.chom.2019.07.006

Walters D, Walsh D, Newton A, Lyon G. Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology. 2005; 95: 1368-73. https://doi.org/10.1094/PHYTO-95-1368

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, et al. Requirement of salicylic acid for the induction of systemic acquired resistance. Science (1979). 1993; 261: 754-6. https://doi.org/10.1126/science.261.5122.754

Durrant WE, Dong X. Systemic acquired resistance. Annu Rev Phytopathol. 2004; 42: 185-209. https://doi.org/10.1146/annurev.phyto.42.040803.140421

Ramsey CL, Freebury PC, Newman DH, Schweigkofler W, Cseke LJ, Newman SE. Use of foliar chemical treatments to induce disease resistance in rhododendrons inoculated with phytophthora ramorum. Glob J Agric Innov Res Dev. 2022; 8: 1-22. https://doi.org/10.15377/2409-9813.2021.08.1

Layman ML, Ramsey C, Schweigkofler W, Newman SE. Field evaluation of a novel, granular soil fumigant for controlling phytophthora ramorum in field nursery soils. Glob J Agric Innov Res Dev. 2020; 7: 12-9. https://doi.org/10.15377/2409-9813.2020.07.2

Cayanan DF, Zheng Y, Zhang P, Graham T, Dixon M, Chong C, et al. Sensitivity of five container-grown nursery species to chlorine in overhead irrigation water. HortScience. 2008; 43: 1882-7. https://doi.org/10.21273/HORTSCI.43.6.1882

Cayanan DF, Zhang P, Liu W, Dixon M, Zheng Y. Efficacy of chlorine in controlling five common plant pathogens. HortScience. 2009; 44: 157-63. https://doi.org/10.21273/HORTSCI.44.1.157

Cayanan DF, Dixon M, Zheng Y, Llewellyn J. Response of container-grown nursery plants to chlorine used to disinfest irrigation water. HortScience. 2009; 44: 164-7. https://doi.org/10.21273/HORTSCI.44.1.164

Kim M, Kumar S, Kwon H, Kim W, Kim Y. Influence of reactive oxygen species produced by chlorine dioxide on induction of insect cell apoptosis. Korean J Appl Entomol. 2016; 5: 267-75. https://doi.org/10.5656/KSAE.2016.07.0.034

Andrés CMC, Lastra JMP de la, Andrés Juan C, Plou FJ, Pérez-Lebeña E. Chlorine dioxide: friend or foe for cell biomolecules? A chemical approach. Int J Mol Sci. 2022; 23(24), 15660. https://doi.org/10.3390/ijms232415660

Vellosillo T, Vicente J, Kulasekaran S, Hamberg M, Castresana C. Emerging complexity in reactive oxygen species production and signaling during the response of plants to pathogens. Plant Physiol. 2010; 154: 444-8. https://doi.org/10.1104/pp.110.161273

Jwa N-S, Hwang BK. Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Front Plant Sci 2017; 8: 1687. https://doi.org/10.3389/fpls.2017.01687

Alvarez ME, Pennell RI, Meijer P-J, Ishikawa A, Dixon RA, Lamb C. Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell. 1998; 92: 773-84. https://doi.org/10.1016/S0092-8674(00)81405-1

Lorenzini G, Guidi L, Nali C, Ciompi S, Soldatini GF. Photosynthetic response of tomato plants to vascular wilt diseases. Plant Sci. 1997; 124: 143-52. https://doi.org/10.1016/S0168-9452(97)04600-1

Nogués S, Cotxarrera L, Alegre L, Trillas MI. Limitations to photosynthesis in tomato leaves induced by Fusarium wilt. New Phytol. 2002; 154: 461-70. https://doi.org/10.1046/j.1469-8137.2002.00379.x

Hampton RE, Wullschleger SD, Oosterhuis DM. Impact of verticillium wilt on net photosynthesis, respiration and photorespiration in field-grown cotton (Gossypium hirsutum L.). Physiol Mol Plant Pathol. 1990; 37: 271-80. https://doi.org/10.1016/0885-5765(90)90076-A

Bassanezi R, Amorim L, Filho AB, Berger R. Gas exchange and emission of chlorophyll fluorescence during the monocycle of rust, angular leaf spot and anthracnose on bean leaves as a function of their trophic characteristics. J Phytopathol. 2002; 150: 37-47. https://doi.org/10.1046/j.1439-0434.2002.00714.x

Weng H, Zeng Y, Cen H, He M, Meng Y, Liu Y, et al. Characterization and detection of leaf photosynthetic response to citrus Huanglongbing from cool to hot seasons in two orchards. Trans ASABE. 2020; 63: 501-12. https://doi.org/10.13031/trans.13469

Brouwer M, Lievens B, Hemelrijck W, Ackerveken G, Cammue BPA, Thomma BPHJ. Quantification of disease progression of several microbial pathogens on Arabidopsis thaliana using real-time fluorescence PCR. FEMS Microbiol Lett. 2003; 228: 241-8. https://doi.org/10.1016/S0378-1097(03)00759-6

Ierna A. Characterization of potato genotypes by chlorophyll fluorescence during plant aging in a Mediterranean environment. Photosynthetica. 2007; 45: 568-75. https://doi.org/10.1007/s11099-007-0097-y

Osdaghi E, Young AJ, Harveson RM. Bacterial wilt of dry beans caused by Curtobacterium flaccumfaciens pv. flaccumfaciens: A new threat from an old enemy. Mol Plant Pathol. 2020; 21: 605-21. https://doi.org/10.1111/mpp.12926

Harveson RM, Schwartz HF, Vidaver AK, Lambrecht PA, Otto KL. New outbreaks of bacterial wilt of dry bean in Nebraska observed from field infections. Plant Dis. 2006; 90: 681-681. https://doi.org/10.1094/PD-90-0681A

Conner RL, Balasubramanian P, Erickson RS, Huang HC, Mündel H-H. Bacterial wilt resistance in kidney beans. Can J Plant Sci. 2008; 88:1109-13. https://doi.org/10.4141/CJPS08074

Yadeta KA, J. Thomma BPH. The xylem as battleground for plant hosts and vascular wilt pathogens. Front Plant Sci. 2013; 4: 1-12. https://doi.org/10.3389/fpls.2013.00097

Sammer UF, Reiher K. Curtobacterium flaccumfaciens pv. flaccumfaciens on Soybean in Germany - A threat for farming. J Phytopathol. 2012; 160: 314-6. https://doi.org/10.1111/j.1439-0434.2012.01902.x

Rajendram D, Ayenza R, Holder FM, Moran B, Long T, Shah HN. Long-term storage and safe retrieval of DNA from microorganisms for molecular analysis using FTA matrix cards. J Microbiol Methods. 2006; 67: 582-92. https://doi.org/10.1016/j.mimet.2006.05.010

Papathanasiou F, Ninou E, Mylonas I, Baxevanos D, Papadopoulou F, Avdikos I, et al. The evaluation of common bean (phaseolus vulgaris L.) genotypes under water stress based on physiological and agronomic parameters. Plants. 2022; 11. https://doi.org/10.3390/plants11182432

Carmona SL, Villarreal-Navarrete A del P, Burbano-David D, Gómez-Marroquín M, Torres-Rojas E, Soto-Suárez M. Boosting photosynthetic machinery and defense priming with chitosan application on tomato plants infected with Fusarium oxysporum f. sp. lycopersici. BioRxiv. Posted August 19, 2020. https://doi.org/10.1101/2020.08.18.256628

Guidi L, Lo Piccolo E, Landi M. Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Front Plant Sci. 2019; 10: 1-11. https://doi.org/10.3389/fpls.2019.00174

Kalaji HM, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, et al. Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynth Res. 2014; 122: 121-58. https://doi.org/10.1007/s11120-014-0024-6

Castillo-Argaez R, Schaffer B, Vazquez A, Sternberg LDSL. Leaf gas exchange and stable carbon isotope composition of redbay and avocado trees in response to laurel wilt or drought stress. Environ Exp Bot. 2020; 171: 103948. https://doi.org/10.1016/j.envexpbot.2019.103948

Yong JWH, Wong SC, Farquhar GD. Stomatal responses to changes in vapour pressure difference between leaf and air. Plant Cell Environ. 1997; 20: 1213-6. https://doi.org/10.1046/j.1365-3040.1997.d01-27.x

Conaty WC, Mahan JR, Neilsen JE, Constable GA. Vapour pressure deficit aids the interpretation of cotton canopy temperature response to water deficit. Funct Plant Biol. 2014; 41: 535-46. https://doi.org/10.1071/FP13223

Yan W, Zhong Y, Shangguan Z. A meta-analysis of leaf gas exchange and water status responses to drought. Sci Rep. 2016; 6: 1-9. https://doi.org/10.1038/srep20917

Jhon MS. The water puzzle and the hexagonal key. Uplifting Press, Inc.; 2004.

Engineering ToolBox. Supercooled water - vapor pressure vs. temperature. Undercooled Water and Vapor Pressure 2014. https://www.engineeringtoolbox.com/water-supercooled-vapor-pressure-d_1910.html (accessed April 15, 2023).

Ramsey CL. Application of a structured water generator for crop irrigation: Structured water, drought tolerance, and alteration of plant defense mechanisms to abiotic stressors. J Basic Appl Sci. 2021; 17: 127-52. https://doi.org/10.29169/1927-5129.2021.17.14

Yang W. Effect of chlorine dioxide gas treatment on bacterial inactivation inoculated on spinach leaves and on pigment content (Thesis). Ohio State University; 2015.

Pollack GH. Cell electrical properties: reconsidering the origin of the electrical potential. Cell Biol Int. 2015; 39: 237-42. https://doi.org/10.1002/cbin.10382

Pollack GH. The fourth phase of water. In: Bakhru A, Nutrition and Integrative Medicine, Seattle: Ebner & Sons Publishers; 2013. https://doi.org/10.1201/9781315153155-18

Pollack G, Figueroa X, Zhao Q. Molecules, water, and radiant energy: new clues for the origin of life. Int J Mol Sci. 2009; 10: 1419-29. https://doi.org/10.3390/ijms10041419

Chai B, Yoo H, Pollack GH. Effect of radiant energy on near-surface water. J Phys Chem B. 2009; 13(42): 13953-8.

Dumanović J, Nepovimova E, Natić M, Kuča K, Jaćević V. The significance of reactive oxygen species and antioxidant defense system in plants: A concise overview. Front Plant Sci. 2021; 11: 552969. https://doi.org/10.3389/fpls.2020.552969

Ho M-W. Illuminating water and life: Emilio Del Giudice. Electromagn Biol Med. 2015; 34: 113-22. https://doi.org/10.3109/15368378.2015.1036079

Ho M. Superconducting quantum coherent water in nanospace confirmed. Sci Soc. 2012; 55: 48-51.

Ho M. Life is water electric. Bioelectromagnetic and Subtle Energy Medicine, vol. 19, 2014.

Joardder MUH, Mourshed M, Hasan Masud M. State of bound water: measurement and significance in food processing. Cham: Springer International Publishing; 2019. https://doi.org/10.1007/978-3-319-99888-6

Messori C. Deep into the water: exploring the hydro-electromagnetic and quantum-electrodynamic properties of interfacial water in living systems. OAlib. 2019; 06: 1-50. https://doi.org/10.4236/oalib.1105435

Messori C. The super-coherent state of biological water. OAlib. 2019; 06: 1-5. https://doi.org/10.4236/oalib.1105236

Giudice ED, Voeikov V, Tedeschi A, Vitiello G. The origin and the special role of coherent water in living systems. In: Fels D, Cifra M, Scholkmann F, Eds., Fields of the Cell. 2015, pp. 95-111.

Giudice ED, Tedeschi A, Vitiello G, Voeikov V. Coherent structures in liquid water close to hydrophilic surfaces. J Phys Conf Ser 2013; 442: 012028. https://doi.org/10.1088/1742-6596/442/1/012028

Giudice E Del, Spinetti PR, Tedeschi A. Water dynamics at the root of metamorphosis in living organisms. Water (Basel). 2010; 2: 566-86. https://doi.org/10.3390/w2030566

Bono I, Del Giudice E, Gamberale L, Henry M. Emergence of the coherent structure of liquid water. Water (Basel). 2012; 4: 510-32. https://doi.org/10.3390/w4030510

Rascio A. Bound water in plants and its relationships to the abiotic. Rec Res Dev Plant Physiol. 1997; 1: 215-22.

Rascio A, Russo M, Platani C, Di Fonzo N. Drought intensity effects on genotypic differences in tissue affinity for strongly bound water. Plant Sci. 1998; 132: 121-6. https://doi.org/10.1016/S0168-9452(98)00006-5

Jiao S, Zeng F, Huang Y, Zhang L, Mao J, Chen B. Physiological, biochemical and molecular responses associated with drought tolerance in grafted grapevine. BMC Plant Biol. 2023; 23: 110. https://doi.org/10.1186/s12870-023-04109-x

Zhou HY, Li SG, Li XR, Zhao AF, Zhao HL, Fan HW, et al. Ecophysiological evidence for the competition strategy of two psammophytes Artemisia halodendron and A. frigida in Horqin sandy land, Nei Mongol. Acta Bot Sin. 2004; 46: 284-93.

Kuroki S, Tsenkova R, Moyankova D, Muncan J, Morita H, Atanassova S, et al. Water molecular structure underpins extreme desiccation tolerance of the resurrection plant Haberlea rhodopensis. Sci Rep. 2019; 9: 1-2. https://doi.org/10.1038/s41598-019-39443-4

Sidorenko G, Brilly M, Laptev B, Gorlenko N, Antoshkin L, Vidmar A, et al. The role of modification of the structure of water and water-containing systems in changing their biological, Therapeutic, and other properties overview. Water (Basel). 2021; 13: 2441. https://doi.org/10.3390/w13172441

Sirohiwal A, Pantazis DA. Functional water networks in fully hydrated photosystem II. J Amer Chem Soc. 2022; 144: 22035-50. https://doi.org/10.1021/jacs.2c09121

Sakashita N, Ishikita H, Saito K. Rigidly hydrogen-bonded water molecules facilitate proton transfer in photosystem II. PhysChemChemPhys. 2020; 22: 15831-41. https://doi.org/10.1039/D0CP00295J

Guerra F, Siemers M, Mielack C, Bondar A-N. Dynamics of long-distance hydrogen-bond networks in photosystem II. J Phy Chem B. 2018; 122: 462541. https://doi.org/10.1021/acs.jpcb.8b00649

Hasanuzzaman M, Bhuyan MHM, Zulfiqar F, Raza A, Mohsin S, Mahmud J, et al. Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the rrucial role of a universal defense regulator. Antioxidants. 2020; 9: 681. https://doi.org/10.3390/antiox9080681

Stekhin A, Yakovleva G, Pronko K, Zemskov V. Quantum biophysics of water. Clin Pract. 2018; 15: 579-86. https://doi.org/10.4172/clinical-practice.1000393

Ball P. Water is an active matrix of life for cell and molecular biology. Proc Nat Acad Sci. 2017; 114: 13327-35. https://doi.org/10.1073/pnas.1703781114

Tenga AZ, Marie BA, Ormrod DP. Leaf greenness meter to assess ozone injury to tomato leaves. HortScience. 1989; 24(3): 514. https://doi.org/10.21273/HORTSCI.24.3.514

Guidi L, Nali C, Ciompi S, Lorenzini G, Soldatini GF. The use of chlorophyll fluorescence and leaf gas exchange as methods for studying the different responses to ozone of two bean cultivars. J Exp Bot. 1997; 48: 173-9. https://doi.org/10.1093/jxb/48.1.173

Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, et al. Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res. 2017; 132: 13-66. https://doi.org/10.1007/s11120-016-0318-y

Rodríguez-Moreno L, Pineda M, Soukupová J, Macho AP, Beuzón CR, Barón M, et al. Early detection of bean infection by Pseudomonas syringae in asymptomatic leaf areas using chlorophyll fluorescence imaging. Photosynth Res. 2008; 96: 27-35. https://doi.org/10.1007/s11120-007-9278-6

Kim JH, Bhandari SR, Chae SY, Cho MC, Lee JG. Application of maximum quantum yield, a parameter of chlorophyll fluorescence, for early determination of bacterial wilt in tomato seedlings. Hortic Environ Biotechnol. 2019; 60: 821-9. https://doi.org/10.1007/s13580-019-00182-0

Ivanov DA, Bernards MA. Chlorophyll fluorescence imaging as a tool to monitor the progress of a root pathogen in a perennial plant. Planta. 2016; 243: 263-79. https://doi.org/10.1007/s00425-015-2427-9

Lotfi R, Ghassemi-Golezani K, Pessarakli M. Salicylic acid regulates photosynthetic electron transfer and stomatal conductance of mung bean (Vigna radiata L.) under salinity stress. Biocatal Agri Biotech. 2020; 26: 101635.

Wang W, Wang X, Zhang J, Huang M, Cai J, Zhou Q, DaiT, Jiang D. Salicylic acid and cold priming induce late-spring freezing tolerance bymaintaining cellular redox homeostasis and protecting photosynthetic apparatus in wheat. Plant Growth Regul. 2020; 90: 109-21.

Sheteiwy MS, An J, Yin M, Jia X, Guan Y, He F, Hu J. Cold plasma treatment and exogenous salicylic acid priming enhances salinity tolerance of Oryza sativa seedlings. Protoplasma 2019; 256: 79-99.

Llorens E, González-Hernández AI, Scalschi L, Fernández-Crespo E, Camañes G, Vicedo B, et al. Priming mediated stress and cross-stress tolerance in plants: Concepts and opportunities. Priming-Mediated Stress and Cross-Stress Tolerance in Crop Plants, Elsevier; 2020, p. 1-20. https://doi.org/10.1016/B978-0-12-817892-8.00001-5

Sherin G, Aswathi KPR, Puthur JT. Photosynthetic functions in plants subjected to stresses are positively influenced by priming. Plant Stress 2022; 4: 100079. https://doi.org/10.1016/j.stress.2022.100079

dos Santos Araújo G, de Oliveira Paula-Marinho S, de Paiva Pinheiro SK, de Castro Miguel E, de Sousa Lopes L, Camelo Marques E, et al. H2O2 priming promotes salt tolerance in maize by protecting chloroplasts ultrastructure and primary metabolites modulation. Plant Sci. 2021; 303: 110774. https://doi.org/10.1016/j.plantsci.2020.110774

Mohammedsani Z. Systemic acquired resistance (SAR) and it’s application in crop plants improvement to biotic stresses: Review. Int J Res Stud Sci Eng Technol. 2018; 5: 17-24.

Maithani D, Singh H, Sharma A. Stress alleviation in plants using SAR and ISR: Current views on stress signaling network. Microbes and Signaling Biomolecules Against Plant Stress: Strategies of Plant-Microbe Relationships for Better Survival, 2021, p. 7-36. https://doi.org/10.1007/978-981-15-7094-0_2

Dutta H, Kumar RG, Borah M. Efficacy of biotic and chemical inducers of SAR in management of plant viruses. Int J Econ Plants. 2019; 6: 130-5. https://doi.org/10.23910/IJEP/2019.6.3.0323

Shine MB, Xiao X, Kachroo P, Kachroo A. Signaling mechanisms underlying systemic acquired resistance to microbial pathogens. Plant Sci. 2019; 279: 81-6. https://doi.org/10.1016/j.plantsci.2018.01.001

Kamle M, Borah R, Bora H, Jaiswal AK, Singh RK, Kumar P. Systemic acquired resistance (SAR) and induced systemic resistance (ISR): role and mechanism of action against phytopathogens. In: Hesham AL, Upadhyay R, Sharma G, Manoharachary C, Gupta V, Eds., Fungal Biotechnology and Bioengineering. Fungal Biology. Cham: Springer; 2020, p. 457-70. https://doi.org/10.1007/978-3-030-41870-0_20

Lukan T, Coll A. Intertwined roles of reactive oxygen species and salicylic acid signaling are crucial for the plant response to biotic stress. Int J Mol Sci. 2022; 23(10): 5568. https://doi.org/10.3390/ijms23105568

Filgueiras CC, Martins AD, Pereira RV, Willett DS. The ecology of salicylic acid signaling: Primary, secondary and tertiary effects with applications in agriculture. Int J Mol Sci. 2019; 20(23): 5851. https://doi.org/10.3390/ijms20235851

Bürger M, Chory J. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe. 2019; 26: 163-72. https://doi.org/10.1016/j.chom.2019.07.006

Peng Y, Yang J, Li X, Zhang Y. Salicylic acid: biosynthesis and signaling. Annu Rev Plant Biol. 2021; 72: 761-91. https://doi.org/10.1146/annurev-arplant-081320-092855

Mishra A, Baek K-H. Salicylic acid biosynthesis and metabolism: A divergent pathway for plants and bacteria. Biomolecules. 2021; 11: 705. https://doi.org/10.3390/biom11050705

Zhang Y, Li X. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr Opin Plant Biol. 2019; 50: 29-36. https://doi.org/10.1016/j.pbi.2019.02.004

Gozzo F, Faoro F. Systemic acquired resistance (50 years after discovery): moving from the lab to the field. J Agric Food Chem. 2013; 61: 12473-91. https://doi.org/10.1021/jf404156x

van Butselaar T, Van den Ackerveken G. Salicylic acid steers the growth-immunity tradeoff. Trends Plant Sci. 2020; 25: 566-76. https://doi.org/10.1016/j.tplants.2020.02.002.

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Copyright (c) 2023 Craig L. Ramsey, Vanessa M. Sandoval, Paul C. Freebury, Debra H. Newman, Greg Dooley, Leland J. Cseke, Steven E. Newman