Salicylic Acid Regulates Systemic Defense Signaling in Chickpea During Fusarium oxysporum f. sp. ciceri Race 1 Infection
- 213 Downloads
Annual loss of productivity of the important crop legume chickpea has received prime scientific concern at recent times. Vascular wilt caused by fungal pathogen Fusarium oxysporum f. sp. ciceris race 1 (Foc1) accounts for major share of yield loss of chickpea. Control of this disease remains a challenge due to the lack of appropriate breeding programs to manage fast pathogen mutability. Previous studies with this pathogen have highlighted the role of reactive oxygen species (ROS) as chemical signal in enkindling downstream systemic resistance response instead of activating site specific defense. But the role of salicylic acid in modulating resistance is still unexplored. Present study explains the probable function of salicylic acid (SA) in coordination with ROS. The external SA application reveals the restoration of relative water content of infected susceptible chickpea plants. The qRT-PCR based expression study of key SA biosynthetic genes indicate that the SA biogenesis takes place by the activity of phenylalanine ammonia lyase (PAL) that activates other SA responsive genes and TGA transcription factors to induce an active defense against Foc1. Finally, detection of SA by LC MS/MS along with the accumulation of transcripts of SA marker genes, PR1 and PR5, strengthens the involvement of SA in translocation of distant systemic signals in chickpea-Foc1 interaction.
KeywordsBiotic stress Cicer arietinum Fusarium oxysporum f. sp. ciceri race 1 Systemic response Salicylic acid Wilt disease
Authors thank Dr. S.C. Pande (ICRISAT, Patancheru) for providing fungal culture and Dr. S.K. Chaturvedi (IIPR, Kanpur) for providing chickpea seeds. Authors are also thankful to Dr. Kaushik Bannerjee, National Research Centre for Grapes, Solapur, Pune, India, for performing the LC MS/MS of the sample. Unwearied assistance of Mr. Swarnava Das for physiological experiments is greatly acknowledged. Mr. Sudipta Basu is duly acknowledged for seed multiplication. Finally, authors acknowledge the Director, Bose Institute for infrastructural facilities.
This work was supported by the grant provided to A.Bhar by Council of Scientific and Industrial Research, India (09/015(0378) /2009-EMR-1) and to M.Chatterjee by Department of Biotechnology, Government of India (BT/01/COE/06/03/2006). The funding organizations had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
- Barrs HD, Kozlowski TT (1968) Determination of water deficits in plant tissues. Water Deficits Plant Growth 1:235–368Google Scholar
- Chatterjee M, Gupta S, Bhar A, Chakraborti D, Basu D, Das S (2014) Analysis of root proteome unravels differential molecular responses during compatible and incompatible interaction between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceri Race1 (Foc1). BMC Genomics 15(1):949. https://doi.org/10.1186/1471-2164-15-949 CrossRefPubMedPubMedCentralGoogle Scholar
- Fock-Bastide I, Palama TL, Bory S, Lécolier A, Noirot M, Joët T (2014) Expression profiles of key phenylpropanoid genes during Vanilla planifolia pod development reveal a positive correlation between PAL gene expression and vanillin biosynthesis. Plant Physiol Biochem 74:304–314. https://doi.org/10.1016/j.plaphy.2013.11.026 CrossRefPubMedGoogle Scholar
- Gayatridevi S, Jayalakshmi SK, Mulimani VH, Sreeramulu K (2013) Salicylic acid and salicylic acid sensitive and insensitive catalases in different genotypes of chickpea against Fusarium oxysporum f. sp. ciceri. Physiol Mol Biol Plants 19(4):529–536. https://doi.org/10.1007/s12298-013-0184-4 CrossRefPubMedPubMedCentralGoogle Scholar
- Gupta S, Chakraborti D, Rangi RK, Basu D, Das S (2009) A molecular insight into the early events of chickpea (Cicer arietinum) and Fusarium oxysporum f. sp. ciceri (race 1) interaction through cDNA-AFLP analysis. Phytopathology 99(11):1245–1257. https://doi.org/10.1094/PHYTO-99-11-1245 CrossRefPubMedGoogle Scholar
- Gupta S, Bhar A, Chatterjee M, Das S (2013) Fusarium oxysporum f. sp. ciceri race 1 induced redox state alterations are coupled to downstream defense signaling in root tissues of chickpea (Cicer arietinum L.) PLoS One 8(9):e73163. https://doi.org/10.1371/journal.pone.0073163 CrossRefPubMedPubMedCentralGoogle Scholar
- Gupta S, Bhar A, Chatterjee M, Ghosh A, Das S (2017) Transcriptomic dissection reveals wide spread differential expression in chickpea during early time points of Fusarium oxysporum f. sp. ciceri race 1 attack. PLoS One 12(5):e0178164. https://doi.org/10.1371/journal.pone.0178164 CrossRefPubMedPubMedCentralGoogle Scholar
- Hennig J, Malamy J, Grynkiewicz G, Indulski J, Klessig DF (1993) Interconversion of the salicylic acid signal and its glucoside in tobacco. Plant J 4(4):593–600. https://doi.org/10.1046/j.1365-313X.1993.04040593.x CrossRefPubMedGoogle Scholar
- Lemos M, Xiao Y, Bjornson M, Wang JZ, Hicks D, Souza A, Wang CQ, Yang P, Ma S, Dinesh-Kumar S, Dehesh K (2016) The plastidial retrograde signal methyl erythritol cyclopyrophosphate is a regulator of salicylic acid and jasmonic acid crosstalk. J Exp Bot 67(5):1557–1566. https://doi.org/10.1093/jxb/erv550 CrossRefPubMedPubMedCentralGoogle Scholar
- Manikandan R, Raguchander T (2014) Fusarium oxysporum f. sp. lycopersici retardation through induction of defensive response in tomato plants using a liquid formulation of Pseudomonas fluorescens (Pf1). Eur J Plant Pathol 140(3):469–480. https://doi.org/10.1007/s10658-014-0481-y CrossRefGoogle Scholar
- Meher HC, Gajbhiye VT, Singh G, Chawla G (2015) Altered metabolomic profile of selected metabolites and improved resistance of Cicer arietinum (L.) against Meloidogyne incognita (Kofoid & White) Chitwood following seed soaking with salicylic acid, benzothiadiazole or nicotinic acid. Acta Physiol Plant 37(7):1–12. https://doi.org/10.1007/s11738-015-1888-6 CrossRefGoogle Scholar
- Saikia R, Yadav M, Singh BP et al (2006) Induction of resistance in chickpea by cell wall protein of Fusarium oxysporum f. sp. ciceri and Macrophomina phaseolina. Curr Sci 91:1543–1546Google Scholar
- Tieman D, Zeigler M, Schmelz E, Taylor MG, Rushing S, Jones JB, Klee HJ (2010) Functional analysis of a tomato salicylic acid methyl transferase and its role in synthesis of the flavor volatile methyl salicylate. Plant J 62(1):113–123. https://doi.org/10.1111/j.1365-313X.2010.04128.x CrossRefPubMedGoogle Scholar
- Umemura K, Satou J, Iwata M, Uozumi N, Koga J, Kawano T, Koshiba T, Anzai H, Mitomi M (2009) Contribution of salicylic acid glucosyltransferase, OsSGT1, to chemically induced disease resistance in rice plants. Plant J 57(3):463–472. https://doi.org/10.1111/j.1365-313X.2008.03697.x CrossRefPubMedGoogle Scholar