Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Novel insights into the Citrus sinensis nonhost response suggest photosynthesis decline, abiotic stress networks and secondary metabolism modifications

Lucas D. Daurelio A F , M. Laura Tondo A , M. Soledad Romero B , Paz Merelo C , Adriana A. Cortadi D , Manuel Talón E , Francisco R. Tadeo E and Elena G. Orellano A F
+ Author Affiliations
- Author Affiliations

A Instituto de Biología Molecular y Celular de Rosario – Consejo Nacional de Investigaciones Científicas y Técnicas), Facultad de Ciencias Bioquímicas y Farmacéuticas (FBIOYF) – Universidad Nacional de Rosario (UNR), Suipacha 531 (S2002 LRK), Rosario, Santa Fe, Argentina.

B Instituto de Agrobiotecnología de Rosario (INDEAR), Ocampo 210 bis, Predio CCT Rosario, (2000), Rosario, Santa Fe, Argentina.

C European Molecular Biology Laboratory, Heidelberg, Meyerhofstraße 1, 69117 Heidelberg, Germany.

D Área de Biología Vegetal, FBIOYF – UNR, Suipacha 531 (S2002 LRK), Rosario, Santa Fe, Argentina.

E Centre de Genómica, Institut Valencià d’Investigacions Agràries, Apt. Oficial, 46113 Montcada, València, Spain.

F Corresponding authors. Emails: daurelio@ibr-conicet.gov.ar; orellano@ibr-conicet.gov.ar

Functional Plant Biology 42(8) 758-769 https://doi.org/10.1071/FP14307
Submitted: 4 November 2014  Accepted: 24 April 2015   Published: 29 May 2015

Abstract

Plants are constantly exposed to stress factors. Biotic stress is produced by living organisms such as pathogens, whereas abiotic stress by unfavourable environmental conditions. In Citrus species, one of the most important fruit crops in the world, these stresses generate serious limitations in productivity. Through biochemical and transcriptomic assays, we had previously characterised the Citrus sinensis (L.) Osbeck nonhost response to Xanthomonas campestris pv. vesicatoria (Doidge), in contrast to Asiatic citrus canker infection caused by Xanthomonas citri subsp. citri (Hasse). A hypersensitive response (HR) including changes in the expression of several transcription factors was reported. Here, a new exhaustive analysis of the Citrus sinensis transcriptomes previously obtained was performed, allowing us to detect the over-representation of photosynthesis, abiotic stress and secondary metabolism processes during the nonhost HR. The broad downregulation of photosynthesis-related genes was correlated with an altered photosynthesis physiology. The high number of heat shock proteins and genes related to abiotic stress, including aquaporins, suggests that stresses crosstalk. Additionally, the secondary metabolism exhibited lignin and carotenoid biosynthesis modifications and expression changes in the cell rescue GSTs. In conclusion, novel features of the Citrus nonhost HR, an important part of the plants’ defence against disease that has yet to be fully exploited in plant breeding programs, are presented.

Additional keywords: canker, hypersensitive response, pathogen, sweet orange, Xanthomonas campestris pv. vesicatoria, Xanthomonas citri subsp. citri.


References

Agrios GN (2005) ‘Plant pathology.’ 5th edn. (Academic Press: San Diego)

Alexandersson E, Danielson JA, Rade J, Moparthi VK, Fontes M, Kjellbom P, Johanson U (2010) Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress. The Plant Journal 61, 650–660.
Transcriptional regulation of aquaporins in accessions of Arabidopsis in response to drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXivVShu7w%3D&md5=d3be7d2ec2aea52d30a8ef66f5a6e6c4CAS | 19947979PubMed |

Backes C, Keller A, Kuentzer J, Kneissl B, Comtesse N, Elnakady YA, Müller R, Meese E, Lenhof H-P (2007) GeneTrail – advanced gene set enrichment analysis. Nucleic Acids Research 35, W186–W192.
GeneTrail – advanced gene set enrichment analysis.Crossref | GoogleScholarGoogle Scholar | 17526521PubMed |

Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFaqsL8%3D&md5=33f955b1e24713e0894a7b2e44b9779aCAS | 18444897PubMed |

Ballester A-R, Lafuente MT, Forment J, Gadea J, De Vos RCH, Bovy AG, González-Candelas L (2011) Transcriptomic profiling of citrus fruit peel tissues reveals fundamental effects of phenylpropanoids and ethylene on induced resistance. Molecular Plant Pathology 12, 879–897.
Transcriptomic profiling of citrus fruit peel tissues reveals fundamental effects of phenylpropanoids and ethylene on induced resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Crsb3I&md5=91aeb8972afa837a90992dc75c231b15CAS | 21726388PubMed |

Bilgin DD, Zavala JA, Zhu J, Clough SJ, Ort DR, DeLucia EH (2010) Biotic stress globally downregulates photosynthesis genes. Plant, Cell & Environment 33, 1597–1613.
Biotic stress globally downregulates photosynthesis genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlemsbbO&md5=21bea668d439e1a2a1256fdede9069c5CAS |

Bolton MD (2009) Primary metabolism and plant defense – fuel for the fire. Molecular Plant—Microbe Interactions 22, 487–497.
Primary metabolism and plant defense – fuel for the fire.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks1Wnsrk%3D&md5=c127c091a13f6355732676f037b59daaCAS | 19348567PubMed |

Cheong YH, Chang HS, Gupta R, Wang X, Zhu T, Luan S (2002) Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiology 129, 661–677.
Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvV2jtrk%3D&md5=2cf0f899e6470b6e37b07d3e990470cfCAS | 12068110PubMed |

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=a79ad41ab909a9e157d9a0478fa85dffCAS | 16497589PubMed |

Cloix C, Jenkins GI (2008) Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin. Molecular Plant 1, 118–128.
Interaction of the Arabidopsis UV-B-specific signaling component UVR8 with chromatin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksVGlu7g%3D&md5=cc4f53574aa69957f4f474f9b383edb6CAS | 20031919PubMed |

Daurelio LD, Checa SK, Barrio JM, Ottado J, Orellano EG (2009) Characterization of Citrus sinensis type 1 mitochondrial alternative oxidase and expression analysis in biotic stress. Bioscience Reports 30, 59–71.
Characterization of Citrus sinensis type 1 mitochondrial alternative oxidase and expression analysis in biotic stress.Crossref | GoogleScholarGoogle Scholar | 19257856PubMed |

Daurelio LD, Petrocelli S, Blanco F, Holuigue L, Ottado J, Orellano EG (2011) Transcriptome analysis reveals novel genes involved in nonhost response to bacterial infection in tobacco. Journal of Plant Physiology 168, 382–391.
Transcriptome analysis reveals novel genes involved in nonhost response to bacterial infection in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntVeltg%3D%3D&md5=6305f773d60306446d7b2d15ffefee8bCAS | 20828873PubMed |

Daurelio LD, Romero MS, Petrocelli S, Merelo P, Cortadi AA, Talon M, Tadeo FR, Orellano EG (2013) Characterization of Citrus sinensis transcription factors closely associated with the non-host response to Xanthomonas campestris pv. vesicatoria. Journal of Plant Physiology 170, 934–942.
Characterization of Citrus sinensis transcription factors closely associated with the non-host response to Xanthomonas campestris pv. vesicatoria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjt1WqsbY%3D&md5=0366c726d5316239d9317432c58423eaCAS | 23453188PubMed |

Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Research 38, W64–W70.
agriGO: a GO analysis toolkit for the agricultural community.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVSqtL0%3D&md5=f0685099a28163f60d93da058613af78CAS | 20435677PubMed |

Dynowski M, Schaaf G, Loque D, Moran O, Ludewig U (2008) Plant plasma membrane water channels conduct the signalling molecule H2O2. The Biochemical Journal 414, 53–61.
Plant plasma membrane water channels conduct the signalling molecule H2O2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptVCisbc%3D&md5=a5bec14edc3bca29431ff1dd792b2ad7CAS | 18462192PubMed |

Gimeno J, Gadea J, Forment J, Perez-Valle J, Santiago J, Martinez-Godoy MA, Yenush L, Belles JM, Brumos J, Colmenero-Flores JM, Talon M, Serrano R (2009) Shared and novel molecular responses of mandarin to drought. Plant Molecular Biology 70, 403–420.
Shared and novel molecular responses of mandarin to drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntVSqsbg%3D&md5=d5ac95514886daa35376661e15e9a871CAS | 19290483PubMed |

Göhre V, Jones AM, Sklenář J, Robatzek S, Weber AP (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Molecular Plant—Microbe Interactions 25, 1083–1092.
Molecular crosstalk between PAMP-triggered immunity and photosynthesis.Crossref | GoogleScholarGoogle Scholar | 22550958PubMed |

Hanssen IM, van Esse HP, Ballester AR, Hogewoning SW, Parra NO, Paeleman A, Lievens B, Bovy AG, Thomma BP (2011) Differential tomato transcriptomic responses induced by pepino mosaic virus isolates with differential aggressiveness. Plant Physiology 156, 301–318.
Differential tomato transcriptomic responses induced by pepino mosaic virus isolates with differential aggressiveness.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVWgtLw%3D&md5=4078eea50dc5e5485bc2f0f496b78bc6CAS | 21427280PubMed |

Hara M, Shinoda Y, Tanaka Y, Kuboi T (2009) DNA binding of citrus dehydrin promoted by zinc ion. Plant, Cell & Environment 32, 532–541.
DNA binding of citrus dehydrin promoted by zinc ion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvVanur8%3D&md5=b7d1c6e23cab873961e9a47cbb00dca0CAS |

Hutin C, Nussaume L, Moise N, Moya I, Kloppstech K, Havaux M (2003) Early light-induced proteins protect Arabidopsis from photooxidative stress. Proceedings of the National Academy of Sciences of the United States of America 100, 4921–4926.
Early light-induced proteins protect Arabidopsis from photooxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjt12nt7g%3D&md5=88045040f1fa851a8edc234f3813a8d6CAS | 12676998PubMed |

Jones JD, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=d47653598b0e63883374f76c0be21a8bCAS | 17108957PubMed |

Kangasjarvi S, Neukermans J, Li S, Aro EM, Noctor G (2012) Photosynthesis, photorespiration, and light signalling in defence responses. Journal of Experimental Botany 63, 1619–1636.
Photosynthesis, photorespiration, and light signalling in defence responses.Crossref | GoogleScholarGoogle Scholar | 22282535PubMed |

Kariola T, Brader G, Helenius E, Li J, Heino P, Palva ET (2006) Early Responsive to Dehydration 15, a negative regulator of abscisic acid responses in Arabidopsis. Plant Physiology 142, 1559–1573.
Early Responsive to Dehydration 15, a negative regulator of abscisic acid responses in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlCns7vK&md5=79b915e29229738e883605f237f1c2aeCAS | 17056758PubMed |

Kauss D, Bischof S, Steiner S, Apel K, Meskauskiene R (2012) FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway. FEBS Letters 586, 211–216.
FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg++-branch of this pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFSnsb0%3D&md5=0a79e861cb93b0d3e33ba37958755a02CAS | 22212719PubMed |

Kerk D, Bulgrien J, Smith DW, Gribskov M (2003) Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria. Plant Physiology 131, 1209–1219.
Arabidopsis proteins containing similarity to the universal stress protein domain of bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisFelsr0%3D&md5=f318a3cee60b00b093d88ac3f27d36deCAS | 12644671PubMed |

Kloepper JW, Ryu C-M, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94, 1259–1266.
Induced systemic resistance and promotion of plant growth by Bacillus spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVWlurbL&md5=f1f9c497c12afaa14d23cad90969b2bdCAS | 18944464PubMed |

Kraiselburd I, Daurelio LD, Tondo ML, Merelo P, Cortadi AA, Talon M, Tadeo FR, Orellano EG (2013) The LOV protein of Xanthomonas citri subsp. citri plays a significant role in the counteraction of plant immune responses during citrus canker. PLoS ONE 8, e80930
The LOV protein of Xanthomonas citri subsp. citri plays a significant role in the counteraction of plant immune responses during citrus canker.Crossref | GoogleScholarGoogle Scholar | 24260514PubMed |

Krupková E, Immerzeel P, Pauly M, Schmülling T (2007) The Tumorous Shoot Development2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development. The Plant Journal 50, 735–750.
The Tumorous Shoot Development2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and co-ordinated plant development.Crossref | GoogleScholarGoogle Scholar | 17461780PubMed |

Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. In ‘Methods in enzymology. Vol. 148.’ (Ed. RD Lester Packer.) pp. 350–382. (Academic Press: London)

Lieberherr D, Wagner U, Dubuis PH, Metraux JP, Mauch F (2003) The rapid induction of glutathione S-transferases AtGSTF2 and AtGSTF6 by avirulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signaling. Plant & Cell Physiology 44, 750–757.
The rapid induction of glutathione S-transferases AtGSTF2 and AtGSTF6 by avirulent Pseudomonas syringae is the result of combined salicylic acid and ethylene signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslGmu78%3D&md5=930e848bdf490ee8bfff3a83eb2dd224CAS |

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–(ΔΔCT) method. Methods (San Diego, Calif.) 25, 402–408.
Analysis of relative gene expression data using real-time quantitative PCR and the 2–(ΔΔCT) method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=322bb6fd44685e306f8210cd65b59997CAS |

Lu L, Du Z, Qin M, Wang P, Lan H, Niu X, Jia D, Xie L, Lin Q, Wu Z (2009) Pc4, a putative movement protein of Rice stripe virus, interacts with a type I DnaJ protein and a small Hsp of rice. Virus Genes 38, 320–327.
Pc4, a putative movement protein of Rice stripe virus, interacts with a type I DnaJ protein and a small Hsp of rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXisFKnu7c%3D&md5=3edbeed2a344283f8290ba39e549cbb1CAS | 19130198PubMed |

Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A (2007) Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum. Plant Physiology 145, 1588–1599.
Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVCntbzE&md5=15ec8d4983d81000d216f478c5992aadCAS | 17965181PubMed |

Makkar HP, Siddhuraju P, Becker K (2007) Plant secondary metabolites. Methods in Molecular Biology (Clifton, N.J.) 393, 1–6.
Plant secondary metabolites.Crossref | GoogleScholarGoogle Scholar |

Martinez-Godoy MA, Mauri N, Juarez J, Marques MC, Santiago J, Forment J, Gadea J (2008) A genome-wide 20 K citrus microarray for gene expression analysis. BMC Genomics 9, 318
A genome-wide 20 K citrus microarray for gene expression analysis.Crossref | GoogleScholarGoogle Scholar | 18598343PubMed |

Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, James C, Papp I, Hortensteiner S, Thomas H, Ougham H (2010) Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytologist 188, 161–174.
Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1aqsLbF&md5=d1a19d84c2aa3a2e606605470c6d2f91CAS | 20704660PubMed |

Mysore KS, Ryu CM (2004) Non-host resistance: how much do we know? Trends in Plant Science 9, 97–104.
Non-host resistance: how much do we know?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOrsr0%3D&md5=c1aef68c7c00f3472dba6b3bd0ad0e8eCAS | 15102376PubMed |

Naoumkina MA, Zhao Q, Gallego-Giraldo L, Dai X, Zhao PX, Dixon RA (2010) Genome-wide analysis of phenylpropanoid defence pathways. Molecular Plant Pathology 11, 829–846.

Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiology 134, 1683–1696.
When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsFKmsbs%3D&md5=0bc1f4acb3adcda7adf917a8d6eb901aCAS | 15047901PubMed |

Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology.’ (Eds S Krawetz, S Misener.) pp. 365–386. (Humana Press: Totowa)

Senthil-Kumar M, Mysore KS (2013) Nonhost resistance against bacterial pathogens: retrospectives and prospects. Annual Review of Phytopathology 51, 407–427.
Nonhost resistance against bacterial pathogens: retrospectives and prospects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFOhtrjK&md5=e2f877f3c1bfdddf8f837c49e8a60723CAS | 23725473PubMed |

Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proceedings of the National Academy of Sciences of the United States of America 101, 8827–8832.
Hydrogen peroxide mediates plant root cell response to nutrient deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkt7w%3D&md5=97c3cab7e27845458519b277f2ea844eCAS | 15173595PubMed |

Song H, Zhao R, Fan P, Wang X, Chen X, Li Y (2009) Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta 229, 955–964.
Overexpression of AtHsp90.2, AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXit1agsbY%3D&md5=342355b5eb9f5c8a2794699aa30920f1CAS | 19148673PubMed |

Talon M, Gmitter FG (2008) Citrus genomics. International Journal of Plant Sciences 2008, 528361

Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. The Plant Journal 37, 914–939.
MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjtFChu78%3D&md5=e83531e3865119c82c8aef4e90d86b21CAS | 14996223PubMed |

Van Bockhaven J, De Vleesschauwer D, Hofte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. Journal of Experimental Botany 64, 1281–1293.
Towards establishing broad-spectrum disease resistance in plants: silicon leads the way.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFKrur4%3D&md5=dafe6de0dd30cf0b9e00c7fe673bc357CAS | 23255278PubMed |

Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. Journal of Experimental Botany 62, 5607–5621.
Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahliae as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFCit7zF&md5=0d0b5c21b7e829a98b7ed77fe474d7ecCAS | 21862479PubMed |

Zou J, Rodriguez-Zas S, Aldea M, Li M, Zhu J, Gonzalez DO, Vodkin LO, DeLucia E, Clough SJ (2005) Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis. Molecular Plant-Microbe Interactions 18, 1161–1174.
Expression profiling soybean response to Pseudomonas syringae reveals new defense-related genes and rapid HR-specific downregulation of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFGqtLbK&md5=69ecf8a2eb2945d6f002da845bcfd396CAS | 16353551PubMed |