Phosphite-induced reactive oxygen species production and ethylene and ABA biosynthesis, mediate the control of Phytophthora capsici in pepper (Capsicum annuum)
Peiqing Liu A C , Benjin Li A C , Ming Lin B , Guoliang Chen B , Xueling Ding A C , Qiyong Weng A C D and Qinghe Chen A B C D
+ Author Affiliations
- Author Affiliations
A Institute of Plant Protection, Fujian Academy of Agricultural Sciences, Fuzhou, 350 003, China.
B Fujian-Taiwan Joint Innovative Centre for Ecological Control of Crop Pests, Fujian Agriculture and Forestry University, Fuzhou 350 002, China.
C Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests, Institute of Plant Protection, Fujian Academy of Agricultural Sciences, Fuzhou, 350 003, China.
D Corresponding authors. Emails: wengqy@faas.cn; chenqh@faas.cn
Functional Plant Biology 43(6) 563-574 https://doi.org/10.1071/FP16006
Submitted: 7 January 2016 Accepted: 15 April 2016 Published: 12 May 2016
Abstract
Phytophthora capsici is an oomycete pathogen with a broad host range that inflicts significant damage in vegetables. Phosphite (Phi) is used to control oomycete diseases, but the molecular mechanisms underlying Phi-induced resistance to P. capsici are unknown. Thus, Phi-inhibited mycelial growth on strain LT1534 and primed host defence were analysed. We demonstrated that Phi (>5 µg mL–1) had a direct antibiotic effect on mycelial growth and zoospore production, and that mortality and DNA content were significantly reduced by pre-treatment with Phi. In addition, elevated hydrogen peroxide (H2O2) promoted callose deposition and increased the levels of soluble proteins and Capsicum annuum L. pathogenesis-related 1 (CaPR1) expression. Furthermore, Phi (1 g L–1) significantly increased the transcription of the antioxidant enzyme genes, and the genes involved in ethylene (ET) and abscisic acid (ABA) biosynthesis, as well as mitogen-activated protein kinase (MAPK) cascades. However, pre-treatment with reactive oxygen species (ROS), ABA and ET biosynthesis inhibitors decreased Phi-induced resistance and reduced the expression of ABA-responsive 1 (CaABR1) and lipoxygenase 1 (CaLOX1). In addition, the decreased ROS and ABA inhibited Phi-induced expression of CaMPK17–1. We propose that Phi-induced ROS production, ET and ABA biosynthesis mediate the control of P. capsici, and that ABA functions through CaMPK17–1-mediated MAPK signalling.
Additional keywords: ET, ABA, phosphite, ROS.
References
Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. Journal of Experimental Botany 65, 1229–1240.| ROS as key players in plant stress signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXks12htLg%3D&md5=a11b4dee4918b474eb8d540f2f4eed2aCAS | 24253197PubMed |
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=436242ae9b449e7335b086f00b7e6e5fCAS | 942051PubMed |
Chacón-López A, Ibarra-Laclette E, Sánchez-Calderón L, Gutiérrez-Alanís D, Herrera-Estrella L (2011) Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation. Plant Signaling & Behavior 6, 382–392.
| Global expression pattern comparison between low phosphorus insensitive 4 and WT Arabidopsis reveals an important role of reactive oxygen species and jasmonic acid in the root tip response to phosphate starvation.Crossref | GoogleScholarGoogle Scholar |
Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S (2011) The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS One 6, e16608
| The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhslyiu7w%3D&md5=70d4b977bd63e21f2009eb833e8a46deCAS | 21304602PubMed |
Chen JP, Tai CY, Chen BH (2004) Improved liquid chromatographic method for determination of carotenoids in Taiwanese mango (Mangifera indica L.). Journal of Chromatography. A 1054, 261–268.
| Improved liquid chromatographic method for determination of carotenoids in Taiwanese mango (Mangifera indica L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos12jsb0%3D&md5=d863f821faf8b6d58aba4deb70345d8aCAS | 15553152PubMed |
Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiology 145, 890–904.
| Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlemsrbN&md5=fb10d4299cf471c5b9b70ad0a64bb031CAS | 17905862PubMed |
Cohen Y, Rubin AE, Vaknin M (2011) Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce. European Journal of Plant Pathology 130, 13–27.
| Post infection application of DL-3-amino-butyric acid (BABA) induces multiple forms of resistance against Bremia lactucae in lettuce.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVOrtrY%3D&md5=1eeb8d1fd3b3fc02c460683f1226ec37CAS |
Dalio RJ, Fleischmann F, Humez M, Osswald W (2014) Phosphite protects Fagus sylvatica seedlings towards Phytophthora plurivora via local toxicity, priming and facilitation of pathogen recognition. PLoS One 9, e87860
| Phosphite protects Fagus sylvatica seedlings towards Phytophthora plurivora via local toxicity, priming and facilitation of pathogen recognition.Crossref | GoogleScholarGoogle Scholar | 24489973PubMed |
Daniel R, Guest D (2006) Defence responses induced by potassium phosphonate in Phytophthora palmivora-challenged Arabidopsis thaliana. Physiological and Molecular Plant Pathology 67, 194–201.
| Defence responses induced by potassium phosphonate in Phytophthora palmivora-challenged Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Eshraghi L, Anderson J, Aryamanesh N, Shearer B, McComb J, Hardy G, O’Brien P (2011) Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathology 60, 1086–1095.
| Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Glt7vE&md5=c13007d1430d02d3512d41b2aabf1ddfCAS |
Eshraghi L, Anderson JP, Aryamanesh N, McComb JA, Shearer B, Hardy GESJ (2014) Defence signalling pathways involved in plant resistance and phosphite-mediated control of Phytophthora cinnamomi. Plant Molecular Biology Reporter 32, 342–356.
| Defence signalling pathways involved in plant resistance and phosphite-mediated control of Phytophthora cinnamomi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXivF2jsL8%3D&md5=6692c27abb87520bab85ce0c1cc4e8a8CAS |
Flors V, Ton J, Jakab G, Mauch‐Mani B (2005) Abscisic acid and callose: team players in defence against pathogens? Journal of Phytopathology 153, 377–383.
| Abscisic acid and callose: team players in defence against pathogens?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXps1Krtr8%3D&md5=a3fb1aa709c50c962003d128c1e18705CAS |
Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Current Opinion in Plant Biology 9, 436–442.
| Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks.Crossref | GoogleScholarGoogle Scholar | 16759898PubMed |
Groves E, Howard K, Hardy G, Burgess T (2015) Role of salicylic acid in phosphite-induced protection against oomycetes; a Phytophthora cinnamomi–Lupinus augustifolius model system. European Journal of Plant Pathology 141, 559–569.
| Role of salicylic acid in phosphite-induced protection against oomycetes; a Phytophthora cinnamomi–Lupinus augustifolius model system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVertrvN&md5=fb22f9d8def9a70679b3e1048a546227CAS |
Hao G, Du X, Zhao F, Ji H (2010) Fungal endophytes-induced abscisic acid is required for flavonoid accumulation in suspension cells of Ginkgo biloba. Biotechnology Letters 32, 305–314.
| Fungal endophytes-induced abscisic acid is required for flavonoid accumulation in suspension cells of Ginkgo biloba.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmvVKlsQ%3D%3D&md5=9e538f8eaeed08fca7eaa889629e16c7CAS | 19821072PubMed |
Jisha K, Puthur JT (2016) Seed priming with BABA (β-amino butyric acid): a cost-effective method of abiotic stress tolerance in Vigna radiata (L.) Wilczek. Protoplasma 253, 277–289.
| Seed priming with BABA (β-amino butyric acid): a cost-effective method of abiotic stress tolerance in Vigna radiata (L.) Wilczek.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlvFWmsL0%3D&md5=2522f2199065b37deb62a10b17ab7698CAS | 25837010PubMed |
Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS, Dalio RJ, Roy SG, Schena L, Zambounis A, Panabières F (2015) The top 10 oomycete pathogens in molecular plant pathology. Molecular Plant Pathology 16, 413–434.
| The top 10 oomycete pathogens in molecular plant pathology.Crossref | GoogleScholarGoogle Scholar | 25178392PubMed |
Kromann P, Pérez WG, Taipe A, Schulte-Geldermann E, Sharma BP, Andrade-Piedra JL, Forbes GA (2012) Use of phosphonate to manage foliar potato late blight in developing countries. Plant Disease 96, 1008–1015.
| Use of phosphonate to manage foliar potato late blight in developing countries.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGlurvM&md5=f9a11c83034c9c4c823e6cd1ef13c193CAS |
Lan C, Liu P, Li B, Chen Q, Weng Q (2013) Development of a specific PCR assay for the rapid and sensitive detection of Phytophthora capsici. Australasian Plant Pathology 42, 379–384.
| Development of a specific PCR assay for the rapid and sensitive detection of Phytophthora capsici.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFeku70%3D&md5=faf0536cde300b919427eba63cea283fCAS |
Lee JY, Kim BS, Lim SW, Lee BK, Kim CH, Hwang BK (1999) Field control of Phytophthora blight of pepper plants with antagonistic rhizobacteria and DL-β-aminon-butyric acid. Plant Pathology 15, 217–222.
Lee BK, Kim BS, Chang SW, Hwang BK (2001) Aggressiveness to pumpkin cultivars of isolates of Phytophthora capsici from pumpkin and pepper. Plant Disease 85, 497–500.
| Aggressiveness to pumpkin cultivars of isolates of Phytophthora capsici from pumpkin and pepper.Crossref | GoogleScholarGoogle Scholar |
Li CX, Wang GX (2004) Interactions between reactive oxygen species, ethylene and polyamines in leaves of Glycyrrhiza inflata seedlings under root osmotic stress. Plant Growth Regulation 42, 55–60.
| Interactions between reactive oxygen species, ethylene and polyamines in leaves of Glycyrrhiza inflata seedlings under root osmotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpslSrtA%3D%3D&md5=13ab0d6608de4e7346400c57f31653f9CAS |
Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLOS Genetics 8, e1002767
| Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVWrurY%3D&md5=ce9da05ce2180c7e046ac0add4204823CAS | 22761583PubMed |
Liu ZQ, Qiu AL, Shi LP, Cai JS, Huang XY, Yang S, Wang B, Shen L, Huang MK, Mou SL, Ma XL, Liu YY, Lin L, Wen JY, Tang Q, Shi W, Guan DY, Lai Y, He SL (2015a) SRC2–1 is required in PcINF1-induced pepper immunity by acting as an interacting partner of PcINF1. Journal of Experimental Botany 66, 3683–3698.
| SRC2–1 is required in PcINF1-induced pepper immunity by acting as an interacting partner of PcINF1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xkt1Kls78%3D&md5=a0d35aae14c9b0338c674b662fe4b3f9CAS | 25922484PubMed |
Liu Z, Shi L, Liu Y, Tang Q, Shen L, Yang S, Cai J, Yu H, Wang R, Wen J (2015b) Genome-wide identification and transcriptional expression analysis of mitogen-activated protein kinase and mitogen-activated protein kinase kinase genes in Capsicum annuum. Frontiers in Plant Science 6, 780
| Genome-wide identification and transcriptional expression analysis of mitogen-activated protein kinase and mitogen-activated protein kinase kinase genes in Capsicum annuum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitFags7%2FM&md5=77d83c458f5f931f4a3cf44353604280CAS | 26442088PubMed |
Machinandiarena MF, Lobato MC, Feldman ML, Daleo GR, Andreu AB (2012) Potassium phosphite primes defense responses in potato against Phytophthora infestans. Journal of Plant Physiology 169, 1417–1424.
| Potassium phosphite primes defense responses in potato against Phytophthora infestans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptFagsrs%3D&md5=77b4a52fad12fef5beb147e8826af214CAS | 22727804PubMed |
Martín‐Rodríguez JÁ, León‐Morcillo R, Vierheilig H, Ocampo JA, Ludwig‐Müller J, García‐Garrido JM (2011) Ethylene‐dependent/ethylene‐independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytologist 190, 193–205.
| Ethylene‐dependent/ethylene‐independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi.Crossref | GoogleScholarGoogle Scholar | 21232061PubMed |
Martínez-Andújar C, Ordiz MI, Huang Z, Nonogaki M, Beachy RN, Nonogaki H (2011) Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy. Proceedings of the National Academy of Sciences of the United States of America 108, 17225–17229.
| Induction of 9-cis-epoxycarotenoid dioxygenase in Arabidopsis thaliana seeds enhances seed dormancy.Crossref | GoogleScholarGoogle Scholar | 21969557PubMed |
Massoud K, Barchietto T, Le Rudulier T, Pallandre L, Didierlaurent L, Garmier M, Ambard-Bretteville F, Seng J-M, Saindrenan P (2012) Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiology 159, 286–298.
| Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2gs7s%3D&md5=11871c497728d8df87351c3ddd1579a7CAS | 22408091PubMed |
Mauch-Mani B, Mauch F (2005) The role of abscisic acid in plant–pathogen interactions. Current Opinion in Plant Biology 8, 409–414.
| The role of abscisic acid in plant–pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsFGgtrY%3D&md5=2f828a1c15ec6a2f187d3dd1c6b060abCAS | 15939661PubMed |
Nahar K, Kyndt T, Nzogela YB, Gheysen G (2012) Abscisic acid interacts antagonistically with classical defense pathways in rice–migratory nematode interaction. New Phytologist 196, 901–913.
| Abscisic acid interacts antagonistically with classical defense pathways in rice–migratory nematode interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKrt7jN&md5=35ffd7a0811a7e2c32d18019865e8e7aCAS | 22985247PubMed |
Niere J, DeAngelis G, Grant B (1994) The effect of phosphonate on the acid-soluble phosphorus components in the genus Phytophthora. Microbiology 140, 1661–1670.
| The effect of phosphonate on the acid-soluble phosphorus components in the genus Phytophthora.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlt1Oksbw%3D&md5=e393ea114ee0cdcf77df11f4cd6e54b7CAS |
Núñez-Pastrana R, Arcos-Ortega GF, Souza-Perera RA, Sánchez-Borges CA, Nakazawa-Ueji YE, García-Villalobos FJ, Guzmán-Antonio AA, Zúñiga-Aguilar JJ (2011) Ethylene, but not salicylic acid or methyl jasmonate, induces a resistance response against Phytophthora capsici in Habanero pepper. European Journal of Plant Pathology 131, 669–683.
| Ethylene, but not salicylic acid or methyl jasmonate, induces a resistance response against Phytophthora capsici in Habanero pepper.Crossref | GoogleScholarGoogle Scholar |
Ogawa-Ohnishi M, Matsushita W, Matsubayashi Y (2013) Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana. Nature Chemical Biology 9, 726–730.
| Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVeru7fP&md5=d5907ad79d90fae46b5f6d7e4b64aa1dCAS | 24036508PubMed |
Ristaino JB, Larkin RP, Campbell CL (1993) Spatial and temporal dynamics of Phytophthora epidemics in commercial bell pepper fields. Phytopathology 83, 1312–1320.
| Spatial and temporal dynamics of Phytophthora epidemics in commercial bell pepper fields.Crossref | GoogleScholarGoogle Scholar |
Stam R, Howden A, Delgado-Cerezo M, Amaro T, Motion GB, Pham J, Huitema E (2013) Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus. Frontiers in Plant Science 4, 387
| Characterization of cell death inducing Phytophthora capsici CRN effectors suggests diverse activities in the host nucleus.Crossref | GoogleScholarGoogle Scholar | 24155749PubMed |
Wang J-E, Liu K-K, Li D-W, Zhang Y-L, Zhao Q, He Y-M, Gong Z-H (2013) A novel peroxidase CanPOD gene of pepper is involved in defense responses to Phytophtora capsici infection as well as abiotic stress tolerance. International Journal of Molecular Sciences 14, 3158–3177.
| A novel peroxidase CanPOD gene of pepper is involved in defense responses to Phytophtora capsici infection as well as abiotic stress tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjtVSqsro%3D&md5=512bb52089ce878ab813451de1b2b745CAS | 23380961PubMed |
Wi SJ, Ji NR, Park KY (2012) Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants. Plant Physiology 159, 251–265.
| Synergistic biosynthesis of biphasic ethylene and reactive oxygen species in response to hemibiotrophic Phytophthora parasitica in tobacco plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntV2gs70%3D&md5=2528304ed61a91dd59d555165abdc08bCAS | 22388490PubMed |
Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA‐induced CAT1 expression and H2O2 production via AtMPK6‐coupled signaling in Arabidopsis. The Plant Journal 54, 440–451.
| AtMKK1 mediates ABA‐induced CAT1 expression and H2O2 production via AtMPK6‐coupled signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmt1Wmsbs%3D&md5=1fab9640a015517ba4d003737915e8d6CAS | 18248592PubMed |
Xiong L, Zhu J-K (2003) Regulation of abscisic acid biosynthesis. Plant Physiology 133, 29–36.
| Regulation of abscisic acid biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlait7k%3D&md5=b55c6615b08da4d3dcf4d5dcb17c58a3CAS | 12970472PubMed |
Zhang M, Li Q, Liu T, Liu L, Shen D, Zhu Y, Liu P, Zhou J-M, Dou D (2015) Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiology 167, 164–175.
| Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Wmt7Y%3D&md5=fab8fba6c4b20f68a1f6f26dbd840956CAS | 25424308PubMed |
Zhu C, Yang X, Lv R, Li Z, Ding X, Tyler BM, Zhang X (2016) Phytophthora capsici homologue of the cell cycle regulator SDA1 is required for sporangial morphology, mycelial growth and plant infection. Molecular Plant Pathology 17, 369–387.
| Phytophthora capsici homologue of the cell cycle regulator SDA1 is required for sporangial morphology, mycelial growth and plant infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xks1egsrk%3D&md5=fc5bd1f1c238154e493b75eb791b2f9aCAS | 26095317PubMed |
