The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi
Seed transmission constitutes a major component of the parasitic cycle for several fungal pathogens. However, very little is known concerning fungal or plant genetic factors that impact seed transmission and mechanisms underlying this key biological trait have yet to be clarified. Such lack of available data could be probably explained by the absence of suitable model pathosystem to study plant-fungus interactions during the plant reproductive phase.
Here we report on setting up a new pathosystem that could facilitate the study of fungal seed transmission. Reproductive organs of Arabidopsis thaliana were inoculated with Alternaria brassicicola conidia. Parameters (floral vs fruit route, seed collection date, plant and silique developmental stages) that could influence the seed transmission efficiency were tested to define optimal seed infection conditions. Microscopic observations revealed that the fungus penetrates siliques through cellular junctions, replum and stomata, and into seed coats either directly or through cracks. The ability of the osmosensitive fungal mutant nik1Δ3 to transmit to A. thaliana seeds was analyzed. A significant decrease in seed transmission rate was observed compared to the wild-type parental strain, confirming that a functional osmoregulation pathway is required for efficient seed transmission of the fungus. Similarly, to test the role of flavonoids in seed coat protection against pathogens, a transparent testa Arabidopsis mutant (tt4-1) not producing any flavonoid was used as host plant. Unexpectedly, tt4-1 seeds were infected to a significantly lower extent than wild-type seeds, possibly due to over-accumulation of other antimicrobial metabolites.
The Arabidopsis thaliana-Alternaria brassicicola pathosystem, that have been widely used to study plant-pathogen interactions during the vegetative phase, also proved to constitute a suitable model pathosystem for detailed analysis of plant-pathogen interactions during the reproductive phase. We demonstrated that it provides an excellent system for investigating the impact of different fungal or plant mutations on the seed transmission process and therefore paves the way towards future high-throughput screening of both Arabidopsis and fungal mutant.
- Van den Bosch F, Fraaije BA, van den Berg F, Shaw MW: Evolutionary bi-stability in pathogen transmission mode. Proc Royal Soc B 2010, 277:1735–1742. CrossRef
- Oliver EJ, Thrall PH, Burdon JJ, Ash JE: Vertical disease transmission in the Cakile-Alternaria host-pathogen interaction. Aust J Bot 2001, 49:561–569. CrossRef
- Hewett PD: Septoria nodorum on seedlings and stubble of winter wheat. Trans Br Mycol Soc 1975, 65:7–18. CrossRef
- Baker KF, Smith SH: Dynamics of seed transmission of plant pathogens. Annu Rev Phytopathol 1966, 14:311–332. CrossRef
- Elmer WH: Seeds as vehicles for pathogen importation. Biol Invasions 2001, 3:263–271. CrossRef
- Cappelli C: Seeds: pathogen transmission through. In Encyclopedia of Plant and Crop Science. Boca Raton. Florida: Taylor & Francis; 2007:1142–1147.
- Iacomi-Vasilescu B, Bataillé-Simoneau N, Campion C, Dongo A, Laurent E, Serandat I, Hamon B, Simoneau P: Effect of null mutations in the AbNIK1 gene on saprophytic and parasitic fitness of Alternaria brassicicola isolates highly resistant to dicarboximides fungicides. Plant Pathol 2008, 57:937–947. CrossRef
- Schlaich NL: Arabidopsis thaliana: the model plant to study host-pathogen interactions. Curr Drug Targets 2011, 12:955–966. CrossRef
- Lawrence CB, Mitchell TK, Craven KD, Cho Y, Cramer RA, Kim KH: At death’s door: Alternaria pathogenicity mechanisms. Plant Pathol J 2008, 24:101–111. CrossRef
- Maude RB, Humpherson-Jones FM: Studies on the seed-borne phases of dark leaf spot (Alternaria brassicicola) and grey leaf spot (Alternaria brassicae) of brassicas. Ann Appl Biol 1980, 95:311–319. CrossRef
- Maude RB, Humpherson-Jones FM, Shuring CG: Treatments to control Phoma and Alternaria infections of brassica seeds. Plant Pathol 1984, 33:525–535. CrossRef
- Humpherson-Jones FM: The incidence of Alternaria spp. and Leptosphaeria maculans in commercial brassica seed in the United Kingdom. Plant Pathology 1985, 34:385–390. CrossRef
- Kubota M, Abiko K, Yanagisawa Y, Nishi K: Frequency of Alternaria brassicicola in commercial cabbage seeds in Japan. J Gen Plant Pathol 2006, 72:197–204. CrossRef
- Humpherson-Jones FM, Maude RB: Studies on the epidemiology of Alternaria brassicicola in Brassica oleracea seed production crops. Ann Appl Biol 1982, 100:61–71. CrossRef
- Knox-Davies PS: Relationships between Alternaria brassicicola and Brassica seeds. Trans Br Mycol Soc 1979, 73:235–248. CrossRef
- Maude RB: Seedborne diseases and their control: principles and practice. Wallingford, United Kingdom: CAB International; 1996.
- Singh D: Mathur SB: Histopathology of seed-borne infections. Boca Raton, Florida: CRC Press LLC; 2004. CrossRef
- Dongo A, Bataillé-Simoneau N, Campion C, Guillemette T, Hamon B, Iacomi-Vasilescu B, Katz L, Simoneau P: The group III two-component histidine kinase of filamentous fungi is involved in the fungicidal activity of the bacterial polyketide ambruticin. Appl Environ Microbiol 2009, 75:127–134. CrossRef
- Thomma BPHJ: Alternaria spp.: from general saprophyte to specific parasite. Molecular Plant Pathology 2003, 4:225–236. CrossRef
- Köhl J, van der Wolf JM: Alternaria brassicicola and Xanthomonas campestris pv. campestris in organic seed production of Brassicae: epidemiology and seed infection. Wageningen: Plant Research International 2005. Note 363, [ http://edepot.wur.nl/17130]
- Fan CY, Köller W: Diversity of cutinases from plant pathogenic fungi: differential and sequential expression of cutinolytic esterases by Alternaria brassicicola. FEMS Microbiol Lett 1998, 158:33–38. CrossRef
- Srivastava A, Ohm RA, Oxiles L, Brooks F, Lawrence CB, Grigoriev IV, Cho Y: A zinc finger family transcription factor AbVf19 is required for the induction of a gene subset important for virulence in Alternaria brassicicola. Mol Plant-Microbe Interact 2012, 25:443–452. CrossRef
- Vaughan DA, Kunwar IK, Sinclair JB, Bernard RL: Routes of entry of Alternaria sp. into soybean seed coats. Seed Science and Technology 1988, 16:725–731.
- Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koornneef M, Ausubel FM, Goodman HM: Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant Journal 1995, 8:659–671. CrossRef
- Routaboul JM, Kerhoas L, Debeaujon I, Pourcel L, Caboche M, Einhorn J, Lepiniec L: Flavonoid diversity and biosynthesis in seed of Arabidopsis thaliana. Planta 2006, 224:96–107. CrossRef
- Pourcel L, Routaboul JM, Cheynier V, Lepiniec L, Debeaujon I: Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends Plant Sci 2007, 12:29–36. CrossRef
- Mohamed-Yaseen Y, Barringer SA, Splittstoesser WE, Costanza S: The role of seed coats in seed viability. Bot Rev 1994, 60:246–260. CrossRef
- Böttcher C, von Roepenack-Lahaye E, Schmidt J, Schmotz C, Neumann S, Scheel D, Clemens S: Metabolome analysis of biosynthetic mutants reveals a diversity of metabolic changes and allows identification of a large number of new compounds in Arabidopsis. Plant Physiol 2008, 147:2107–2120. CrossRef
- Sellam A, Iacomi-Vasilescu B, Hudhomme P, Simoneau P: In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol 2007, 56:296–301. CrossRef
- Debeaujon I, Léon-Kloosterziel KM, Koornneef M: Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol 2000, 122:403–413. CrossRef
- Rodríguez G: Lecture Notes on Generalized Linear Models. 2007.
- R Development Core Team: R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2010.
- Truernit E, Haseloff J: A simple way to identify non-viable cells within living plant tissue using confocal microscopy. Plant Methods 2008, 4:15. CrossRef
- Hoch HC, Galvani CD, Szarowski DH, Turner JN: Two new fluorescent dyes applicable for visualization of fungal cell walls. Mycologia 2005, 9:580–588. CrossRef
- The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Online Date
- May 2012
- Online ISSN
- BioMed Central
- Additional Links
- Seed transmission
- Alternaria brassicicola
- Arabidopsis thaliana
- Seed colonization
- Transparent testa
- Osmotic stress
- Author Affiliations
- 1. Université d’Angers, UMR 1345 IRHS, SFR QUASAV, 2 Bd Lavoisier, Angers cedex, F-49045, France
- 2. INRA, UMR 1345 IRHS, 16 Bd Lavoisier, Angers cedex, F-49045, France
- 3. Agrocampus-Ouest, UMR 1345 IRHS, 2 Bd Lavoisier, Angers cedex, F-49045, France
- 4. USAMV, 59 Bd Marasti, Bucharest, Ro-71331, Romania
- 5. Université d’Angers, SCIAM, IBS, 4 rue Larrey, Angers cedex, F-49933, France
- 6. Université d’Angers, SFR QUASAV, IMAC, rue Georges Morel, Beaucouzé cedex, F-49071, France
- 7. INRA, UMR1318 IJPB, Saclay Plant Sciences, Route de Saint-Cyr, Versailles Cedex, 78026, France