Transcriptomic and Metabolomic Analyses Identify a Role for Chlorophyll Catabolism and Phytoalexin During Medicago Nonhost Resistance Against Asian Soybean Rust

Overview

Journal Sci Rep

Specialty Science

Date 2015 Aug 13

PMID 26267598

Citations 22

Authors

Yasuhiro Ishiga

Srinivasa Rao Uppalapati

Upinder S Gill

David Huhman

Yuhong Tang

Kirankumar S Mysore

Affiliations

Soon will be listed here.

Abstract

Asian soybean rust (ASR) caused by Phakopsora pachyrhizi is a devastating foliar disease affecting soybean production worldwide. Understanding nonhost resistance against ASR may provide an avenue to engineer soybean to confer durable resistance against ASR. We characterized a Medicago truncatula-ASR pathosystem to study molecular mechanisms of nonhost resistance. Although urediniospores formed appressoria and penetrated into epidermal cells of M. truncatula, P. pachyrhizi failed to sporulate. Transcriptomic analysis revealed the induction of phenylpropanoid, flavonoid and isoflavonoid metabolic pathway genes involved in the production of phytoalexin medicarpin in M. truncatula upon infection with P. pachyrhizi. Furthermore, genes involved in chlorophyll catabolism were induced during nonhost resistance. We further characterized one of the chlorophyll catabolism genes, Stay-green (SGR), and demonstrated that the M. truncatula sgr mutant and alfalfa SGR-RNAi lines showed hypersensitive-response-like enhanced cell death upon inoculation with P. pachyrhizi. Consistent with transcriptomic analysis, metabolomic analysis also revealed the accumulation of medicarpin and its intermediate metabolites. In vitro assay showed that medicarpin inhibited urediniospore germination and differentiation. In addition, several triterpenoid saponin glycosides accumulated in M. truncatula upon inoculation with P. pachyrhizi. In summary, using multi-omic approaches, we identified a correlation between phytoalexin production and M. truncatula defense responses against ASR.

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References

Pennisi E . Armed and dangerous. Science. 2010; 327(5967):804-5. DOI: 10.1126/science.327.5967.804. View

Hirashima M, Tanaka R, Tanaka A . Light-independent cell death induced by accumulation of pheophorbide a in Arabidopsis thaliana. Plant Cell Physiol. 2009; 50(4):719-29. DOI: 10.1093/pcp/pcp035. View

Slaminko T, Miles M, Frederick R, Bonde M, Hartman G . New Legume Hosts of Phakopsora pachyrhizi Based on Greenhouse Evaluations. Plant Dis. 2019; 92(5):767-771. DOI: 10.1094/PDIS-92-5-0767. View

Shimada C, Lipka V, OConnell R, Okuno T, Schulze-Lefert P, Takano Y . Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol Plant Microbe Interact. 2006; 19(3):270-9. DOI: 10.1094/MPMI-19-0270. View

Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U . Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-64. DOI: 10.1093/biostatistics/4.2.249. View

Zehavi U, Levy M, Naim M, EVRON R, Polacheck I . Synthesis and antifungal activity of medicagenic acid saponins on plant pathogens: modification of the saccharide moiety and the 23 alpha substitution. Carbohydr Res. 1993; 244(1):161-9. DOI: 10.1016/0008-6215(93)80012-4. View

Stukenbrock E, McDonald B . The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol. 2008; 46:75-100. DOI: 10.1146/annurev.phyto.010708.154114. View

Hortensteiner S . Chlorophyll degradation during senescence. Annu Rev Plant Biol. 2006; 57:55-77. DOI: 10.1146/annurev.arplant.57.032905.105212. View

Ishiga Y, Ishiga T, Wangdi T, Mysore K, Uppalapati S . NTRC and chloroplast-generated reactive oxygen species regulate Pseudomonas syringae pv. tomato disease development in tomato and Arabidopsis. Mol Plant Microbe Interact. 2011; 25(3):294-306. DOI: 10.1094/MPMI-05-11-0130. View

10.

Nakao M, Nakamura R, Kita K, Inukai R, Ishikawa A . Non-host resistance to penetration and hyphal growth of Magnaporthe oryzae in Arabidopsis. Sci Rep. 2012; 1:171. PMC: 3240950. DOI: 10.1038/srep00171. View

11.

Ayliffe M, Singh R, Lagudah E . Durable resistance to wheat stem rust needed. Curr Opin Plant Biol. 2008; 11(2):187-92. DOI: 10.1016/j.pbi.2008.02.001. View

12.

Ishiga Y, Uppalapati S, Ishiga T, Elavarthi S, Martin B, Bender C . The phytotoxin coronatine induces light-dependent reactive oxygen species in tomato seedlings. New Phytol. 2008; 181(1):147-160. DOI: 10.1111/j.1469-8137.2008.02639.x. View

13.

Zhou C, Han L, Pislariu C, Nakashima J, Fu C, Jiang Q . From model to crop: functional analysis of a STAY-GREEN gene in the model legume Medicago truncatula and effective use of the gene for alfalfa improvement. Plant Physiol. 2011; 157(3):1483-96. PMC: 3252161. DOI: 10.1104/pp.111.185140. View

14.

Sakuraba Y, Schelbert S, Park S, Han S, Lee B, Andres C . STAY-GREEN and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in Arabidopsis. Plant Cell. 2012; 24(2):507-18. PMC: 3315229. DOI: 10.1105/tpc.111.089474. View

15.

Egusa M, Miwa T, Kaminaka H, Takano Y, Kodama M . Nonhost resistance of Arabidopsis thaliana against Alternaria alternata involves both pre- and postinvasive defenses but is collapsed by AAL-toxin in the absence of LOH2. Phytopathology. 2013; 103(7):733-40. DOI: 10.1094/PHYTO-08-12-0201-R. View

16.

Pruzinska A, Tanner G, Anders I, Roca M, Hortensteiner S . Chlorophyll breakdown: pheophorbide a oxygenase is a Rieske-type iron-sulfur protein, encoded by the accelerated cell death 1 gene. Proc Natl Acad Sci U S A. 2003; 100(25):15259-64. PMC: 299977. DOI: 10.1073/pnas.2036571100. View

17.

Garcia A, Calvo E, de Souza Kiihl R, Harada A, Hiromoto D, Vieira L . Molecular mapping of soybean rust (Phakopsora pachyrhizi) resistance genes: discovery of a novel locus and alleles. Theor Appl Genet. 2008; 117(4):545-53. DOI: 10.1007/s00122-008-0798-z. View

18.

Yorinori J, Paiva W, Frederick R, Costamilan L, Bertagnolli P, Hartman G . Epidemics of Soybean Rust (Phakopsora pachyrhizi) in Brazil and Paraguay from 2001 to 2003. Plant Dis. 2019; 89(6):675-677. DOI: 10.1094/PD-89-0675. View

19.

Hortensteiner S . Stay-green regulates chlorophyll and chlorophyll-binding protein degradation during senescence. Trends Plant Sci. 2009; 14(3):155-62. DOI: 10.1016/j.tplants.2009.01.002. View

20.

Mur L, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E . Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol. 2010; 188(1):161-74. DOI: 10.1111/j.1469-8137.2010.03377.x. View