Plasmalemma localisation of DOUBLE HYBRID PROLINE-RICH PROTEIN 1 and its function in systemic acquired resistance of Arabidopsis thaliana
Ben-Chang Li A B , Chen Zhang A B , Qiu-Xia Chai A B , Yao-Yao Han A , Xiao-Yan Wang A , Meng-Xin Liu A , Huan Feng A and Zi-Qin Xu A C
+ Author Affiliations
- Author Affiliations
A Key Laboratory of Resource Biology and Biotechnology in Western China, Ministry of Education, Provincial Key Laboratory of Biotechnology of Shaanxi, College of Life Sciences, Northwest University, Xi’an 710069, PR China.
B These authors contributed equally to this work.
C Corresponding author. Email: ziqinxu@nwu.edu.cn
Functional Plant Biology 41(7) 768-779 https://doi.org/10.1071/FP13314
Submitted: 26 October 2013 Accepted: 23 January 2014 Published: 11 March 2014
Abstract
The protein encoded by AtDHyPRP1 (DOUBLE HYBRID PROLINE-RICH PROTEIN 1) contains two tandem PRD-8CMs (proline-rich domain-eight cysteine motif) and represents a new type of HyPRPs (hybrid proline-rich proteins). Confocal microscopy to transgenic Arabidopsis plants revealed that AtDHyPRP1-GFP was localised to plasmalemma, especially plasmodesmata. AtDHyPRP1 mainly expressed in leaf tissues and could be induced by salicylic acid, methyl jasmonate, virulent Pseudomonas syringae pv. tomato DC3000 (Pst DC3000) and avirulent P. syringae pv. tomato DC3000 harbouring avrRPM1 (Pst avrRPM1), suggesting it is involved in defence response of Arabidopsis thaliana (L. Heynh.). After treatments with bacterial suspension of virulent Pst DC3000 or conidial suspension of Botrytis cinerea, AtDHyPRP1 overexpressing lines exhibited enhanced resistance, whereas AtDHyPRP1 RNA interference lines became more susceptible to the pathogens with obvious chlorosis or necrosis phenotypes. In systemic acquired resistance (SAR) analyses, distal leaves were challenged with virulent Pst DC3000 after inoculation of the primary leaves with avirulent Pst avrRPM1 (AV) or MgSO4 (MV). Compared with MV, the infection symptoms in systemic leaves of wild-type plants and AtDHyPRP1 overexpressing lines were significantly alleviated in AV treatment, whereas the systemic leaves of AtDHyPRP1 RNAi lines were vulnerable to Pst DC3000, indicating AtDHyPRP1 was functionally associated with SAR.
Additional keywords: hypersensitive response, lipid transfer protein, propidium iodide, quantitative RT-PCR.
References
Blanco-Portales R, López-Raéz JA, Bellido ML, Moyano E, Dorado G, González-Reyes JA, Caballero JL, Muñoz-Blanco J (2004) A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring. Plant Molecular Biology 55, 763–780.| A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlGmtQ%3D%3D&md5=ad69bb1c8212c90ccbd17973c75499dbCAS | 15604715PubMed |
Champigny MJ, Shearer H, Mohammad A, Haines K, Neumann M, Thilmony R, He SY, Fobert P, Dengler N, Cameron RK (2011) Localization of DIR1 at the tissue, cellular and subcellular levels during systemic acquired resistance in Arabidopsis using DIR1:GUS and DIR1:EGFP reporters. BMC Plant Biology 11, 125
| Localization of DIR1 at the tissue, cellular and subcellular levels during systemic acquired resistance in Arabidopsis using DIR1:GUS and DIR1:EGFP reporters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1yqsLvE&md5=c6581dbeda4fd9ba93a5e8fb0cbbcf96CAS | 21896186PubMed |
Chanda B, Xia Y, Mandal MK, Yu K, Sekine KT, Gao QM, Selote D, Hu Y, Stromberg A, Navarre D, Kachroo A, Kachroo P (2011) Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants. Nature Genetics 43, 421–427.
| Glycerol-3-phosphate is a critical mobile inducer of systemic immunity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVOhtb4%3D&md5=fba0690c3cb3b918677640043de8d614CAS | 21441932PubMed |
Chang S, Pikaard CS (2005) Transcript profiling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation. Journal of Biological Chemistry 280, 796–804.
| Transcript profiling in Arabidopsis reveals complex responses to global inhibition of DNA methylation and histone deacetylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtFGnsr%2FJ&md5=73f1426828e869d038e6f0fd4c963366CAS | 15516340PubMed |
Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
| Host-microbe interactions: shaping the evolution of the plant immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Kltbw%3D&md5=ebc8b23e86510cf1aca9d6b7414bf37aCAS | 16497589PubMed |
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16, 735–743.
| Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1M7mvVagsQ%3D%3D&md5=585d6f3bf57d537ce4024156958dfa3aCAS | 10069079PubMed |
Dempsey DA, Klessig DF (2012) SOS – too many signals for systemic acquired resistance? Trends in Plant Science 17, 538–545.
| SOS – too many signals for systemic acquired resistance?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsVWiurs%3D&md5=a8ba35c779163e5d6545cf7e06009cf5CAS | 22749315PubMed |
Dvořáková L, Cvrčková F, Fischer L (2007) Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns. BMC Genomics 8, 412
| Analysis of the hybrid proline-rich protein families from seven plant species suggests rapid diversification of their sequences and expression patterns.Crossref | GoogleScholarGoogle Scholar | 17997832PubMed |
Flor HH (1971) Current status of the gene-for-gene concept. Annual Review of Phytopathology 9, 275–296.
| Current status of the gene-for-gene concept.Crossref | GoogleScholarGoogle Scholar |
Goda H, Sawa S, Asami T, Fujioka S, Shimada Y, Yoshida S (2004) Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiology 134, 1555–1573.
| Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmsLo%3D&md5=e3d2d57a96e046845ef18c9211e490e5CAS | 15047898PubMed |
Guan MX, Chai RH, Kong X, Liu XM (2013) Isolation and characterization of a lipid transfer protein gene (BplLTP1) from Betula platyphylla. Plant Molecular Biology Reporter 31, 991–1001.
| Isolation and characterization of a lipid transfer protein gene (BplLTP1) from Betula platyphylla.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFajtLrF&md5=ff7b264d9189db27d45588f2205e32c6CAS |
Hammerschmidt R (2009) Systemic acquired resistance. Advances in Botanical Research 51, 173–222.
| Systemic acquired resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Slsr%2FK&md5=86eaa0827ba62ea06e36d2075351f1acCAS |
Hammond JP, Bennett MJ, Bowen HC, Broadley MR, Eastwood DC, May ST, Rahn C, Swarup R, Woolaway KE, White PJ (2003) Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants. Plant Physiology 132, 578–596.
| Changes in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslersbo%3D&md5=bd51c17748aae58032eecb6ca096fc77CAS | 12805589PubMed |
José-Estanyol M, Gomis-Rüth FX, Puigdomènech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiology and Biochemistry 42, 355–365.
| The eight-cysteine motif, a versatile structure in plant proteins.Crossref | GoogleScholarGoogle Scholar | 15191737PubMed |
Jung HW, Tschaplinski TJ, Wang L, Glazebrook J, Greenberg JT (2009) Priming in systemic plant immunity. Science 324, 89–91.
| Priming in systemic plant immunity.Crossref | GoogleScholarGoogle Scholar | 19342588PubMed |
Kader JC (1996) Lipid-transfer proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 627–654.
| Lipid-transfer proteins in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtlWgt7w%3D&md5=7234b98fbac630b40511f5f6f0d94e49CAS | 15012303PubMed |
Kamauchi S, Nakatani H, Nakano C, Urade R (2005) Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS Journal 272, 3461–3476.
| Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtFKrurY%3D&md5=94d10ae648e71ad729912e3b95f075a8CAS | 15978049PubMed |
Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130, 2129–2141.
| Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlym&md5=b3c1ad169f659a5c08c8689418961b27CAS | 12481097PubMed |
Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411, 848–853.
| Programmed cell death, mitochondria and the plant hypersensitive response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksF2nsrg%3D&md5=cf5b53d04d40c451679e80c4ce96ce53CAS | 11459068PubMed |
Lopez BR, Tinoco-Ojanguren C, Bacilio M, Mendoza A, Bashan Y (2012) Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks. Environmental and Experimental Botany 81, 26–36.
| Endophytic bacteria of the rock-dwelling cactus Mammillaria fraileana affect plant growth and mobilization of elements from rocks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xmt1Ggtb4%3D&md5=3e453ecd6658cac76a4c2ae435eb9761CAS |
Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419, 399–403.
| A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntlGgsLk%3D&md5=67f32b6c8158e06c5229682bfe548bf6CAS | 12353036PubMed |
Menges M, Hennig L, Gruissem W, Murray JA (2002) Cell cycle-regulated gene expression in Arabidopsis. Journal of Biological Chemistry 277, 41987–42002.
| Cell cycle-regulated gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotF2gtrk%3D&md5=318f3c0fb005cd46f34b69002e713d01CAS | 12169696PubMed |
Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardóczy V, Teige M, Koncz C, Peck S, Bögre L (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. The Plant Journal 48, 485–498.
| The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin.Crossref | GoogleScholarGoogle Scholar | 17059410PubMed |
Mohr PG, Cahill DM (2007) Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato. Functional & Integrative Genomics 7, 181–191.
| Suppression by ABA of salicylic acid and lignin accumulation and the expression of multiple genes, in Arabidopsis infected with Pseudomonas syringae pv. tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1SitLw%3D&md5=4b00f31a6e1869362af3c5b0b908cb82CAS |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bioassays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=727f2209935a898d7e76484915aa5b8dCAS |
Nakamura A, Nakajima N, Goda H, Shimada Y, Hayashi K, Nozaki H, Asami T, Yoshida S, Fujioka S (2006) Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type. The Plant Journal 45, 193–205.
| Arabidopsis Aux/IAA genes are involved in brassinosteroid-mediated growth responses in a manner dependent on organ type.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtV2it7s%3D&md5=377de4647b9ecc2a662891564b7370f4CAS | 16367964PubMed |
Neto LB, de Oliveira RR, Wiebke-Strohm B, Bencke M, Weber RLM, Cabreira C, Abdelnoor RV, Marcelino FC, Zanettini MHB, Passaglia LMP (2013) Identification of the soybean HyPRP family and specific gene response to Asian soybean rust disease. Genetics and Molecular Biology 36, 214–224.
| Identification of the soybean HyPRP family and specific gene response to Asian soybean rust disease.Crossref | GoogleScholarGoogle Scholar | 23885204PubMed |
Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Liu A, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. The Plant Cell 17, 3282–3300.
| Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlersL%2FF&md5=6d62ae78812bac4f61d282c01270d957CAS | 16284307PubMed |
Pagnussat L, Burbach C, Baluska F, de la Canal L (2012) An extracellular lipid transfer protein is relocalized intracellularly during seed germination. Journal of Experimental Botany 63, 6555–6563.
| An extracellular lipid transfer protein is relocalized intracellularly during seed germination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhslakt77J&md5=b46da1177dbaba668b6c913b5ddd431dCAS | 23162115PubMed |
Rounds CM, Lubeck E, Hepler PK, Winship LJ (2011) Propidium iodide competes with Ca2+ to label pectin in pollen tubes and Arabidopsis root hairs. Plant Physiology 157, 175–187.
| Propidium iodide competes with Ca2+ to label pectin in pollen tubes and Arabidopsis root hairs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit7%2FI&md5=9d252b2403a1590ae1fa0a3988122466CAS | 21768649PubMed |
Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
| Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=035d53bacfe5ff4e5166188b3ed6bd8eCAS | 18546601PubMed |
Schultz CJ, Rumsewicz MP, Johnson KL, Jones BJ, Gaspar YM, Bacic A (2002) Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case. Plant Physiology 129, 1448–1463.
| Using genomic resources to guide research directions. The arabinogalactan protein gene family as a test case.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gsLk%3D&md5=fd6e896dd53dac78a40b4280123385fdCAS | 12177459PubMed |
Shah J (2005) Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annual Review of Phytopathology 43, 229–260.
| Lipids, lipases, and lipid-modifying enzymes in plant disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVOksrrP&md5=ac052651e06899c98ba86f4308140dcaCAS | 16078884PubMed |
Stewart CN, Via LE (1993) A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. BioTechniques 14, 748–750.
Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. The Plant Journal 46, 34–53.
| Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjslykt7k%3D&md5=68624b936197e49284885caa410a2d68CAS | 16553894PubMed |
Tian AM, Jiang JJ, Cao JS (2013) Functional analysis of a novel male fertility lipid transfer protein gene in Brassica campestris ssp. Chinensis. Plant Molecular Biology Reporter 31, 775–782.
| Functional analysis of a novel male fertility lipid transfer protein gene in Brassica campestris ssp. Chinensis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFajtLjO&md5=067716b04afdd6729b27911a9d2fc749CAS |
Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal 41, 195–211.
| Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWitrc%3D&md5=0b4301b009febb64f21cb8a5f784888eCAS | 15634197PubMed |
Xiao S, Chye ML (2011) Overexpression of Arabidopsis ACBP3 enhances NPR1-dependent plant resistance to Pseudomonas syringe pv tomato DC3000. Plant Physiology 156, 2069–2081.
| Overexpression of Arabidopsis ACBP3 enhances NPR1-dependent plant resistance to Pseudomonas syringe pv tomato DC3000.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrur3J&md5=5ab722dc422533db491eea75bd33204bCAS | 21670223PubMed |
Yu K, Soares JM, Mandal MK, Wang C, Chanda B, Gifford AN, Fowler JS, Navarre D, Kachroo A, Kachroo P (2013) A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity. Cell Reports 3, 1266–1278.
| A feedback regulatory loop between G3P and lipid transfer proteins DIR1 and AZI1 mediates azelaic-acid-induced systemic immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmt1Cns7g%3D&md5=c9caaa5b61f21248d84077b68063c272CAS | 23602565PubMed |
Zhang Z, Li Q, Li Z, Staswick PE, Wang M, Zhu Y, He Z (2007) Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis–Pseudomonas syringae interaction. Plant Physiology 145, 450–464.
| Dual regulation role of GH3.5 in salicylic acid and auxin signaling during Arabidopsis–Pseudomonas syringae interaction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLrI&md5=dafc64c6d0874b2e205d3dd3548c0842CAS | 17704230PubMed |
