Metabolic determinants in the interaction of biotrophic and hemibiotrophic fungi with cereals
Plant Breeding and Plant Pathology
Final Report Abstract
We have studied the interaction of phytopathogenic fungi with cereal leaves with a focus on three pathosystems involving (hemi)biotrophic fungal pathogens that depend on the provision of nutrients by living host cell in the invaded leaf tissue, namely the biotrophic corn smut fungus Ustilago maydis, the hemibiotrophic maize anthracnose fungus Colletotrichum graminicola and the biotrophic barley powdery mildew fungus, Blumeria graminis f.sp. hordei. Once the provision of carbon and nitrogen building blocks and their utilization depends on host and microbial primary metabolism, respectively, we sought to elucidate which metabolic processes in host and fungal interaction partner have the capability to determine compatibility. The central findings of the project were that Ustilago maydis infected leaves represent strong sinks for carbon and organic nitrogen that outcompete endogenous sinks like growing leaves for organic nitrogen, thereby utterly altering nitrogen allocation in infected maize plants. Increased sink demand for nitrogen was able to increase amino acid exudation from and able to delay senescence of systemic source leaves. Conversely, a smut fungus ∆nit2 GATA transcription factor mutant impaired in the utilization of non-favoured nitrogen sources exhibited reduced virulence, as the germination of sporidia was delayed on planta. In the other pathosystems studied, our interest was focused on the role of central carbon metabolism for the establishment of compatibility. We could identify a C. graminicola mutant that deposits reduced amounts of glycogen into conidiospores due to a defect in an ubiquitin E2 ligase that acts as regulator of carbon metabolism. An elevated percentage of ∆ubc8 mutant conidia failed to produce fully differentiated appressoria, which are the penetration organs used to pierce the host epidermis, leading to reduced pathogenicity of ∆ubc8 mutants. The Colletotrichum higginsianum - Arabidopsis interaction was used to investigate the role of carbon availability in host leaves for susceptibility towards this hemibiotrophic fungus. By the investigation of mutants impaired in central carbohydrate metabolism in different light-dark regimes, we could demonstrate that diurnal carbon turnover in host leaves negatively correlateed with susceptibility towards C. higginsianum and that short periods of carbon limitation could reduce the responsiveness of salicylic acid-triggered defence. In particular, mutants with reduced starch or organic acid turnover prove hypersusceptible towards C. higginsianum. Likewise, we could show that only isoform 2 of cytosolic malic enzyme, ME2, supplies reducing power to the host defence response. Arabidopsis me2 mutants were more susceptible towards C. higginsinaum compared to wild type. Similarly, the suppression of starch biosynthesis in barley by silencing all isoforms of the committed step enzyme, AGPase, resulted in the loss of penetration resistance against the non-adapted wheat powdery mildew fungus. In this pathosystem, overall carbohydrate turnover was not strongly affected, but cell wall composition and the transcriptional defence response towards fungal challenge were aberrant and could account for the observed decrease of non-host resistance.
Publications
- (2008) Infection of maize leaves with Ustilago maydis prevents establishment of C4 photosynthesis. J. Plant Physiol. 165: 19-28
Horst RJ, Engelsdorf T, Sonnewald U, Voll LM
(See online at https://doi.org/10.1016/j.jplph.2007.05.008) - (2008) Reprogramming a maize plant: Transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J., 56: 181-195
Doehlemann G, Wahl R, Horst R, Voll LM, Usadel B, Poree F, Stitt M, Pons-Kühnemann J, Sonnewald U, Kahmann R, Kaemper J
(See online at https://doi.org/10.1111/j.1365-313X.2008.03590.x) - (2009) Manipulation of plant innate immunity and gibberellin as factor of compatibility in the mutualistic association of barley roots with Piriformospora indica. Plant J. 59: 461- 474
Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler P, Scholz U, Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH
(See online at https://doi.org/10.1111/j.1365-313X.2009.03887.x) - (2009) Phytohormones in plant root-Piriformospora indica mutualism. Plant Sig. Behav. 4: 669-671
Schäfer P, Pfiffi S, Voll LM, Zajic D, Chandler P, Scholz U, Pons-Kühnemann J, Sonnewald S, Sonnewald U, Kogel KH
(See online at https://doi.org/10.4161/psb.4.7.9038) - (2010) A model of Ustilago maydis leaf tumor metabolism. Plant Sig. Behav. 5 (11): 1446-1449
Horst RJ, Doehlemann G, Wahl R, Hofmann J, Schmiedl A, Kahmann R, Kämper J, Voll LM
(See online at https://doi.org/10.4161/psb.5.11.13360) - (2010) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152: 293-308
Horst RJ, Doehlemann G, Wahl R, Kahmann R, Kämper J, Sonnewald U, Voll LM
(See online at https://doi.org/10.1104/pp.109.147702) - (2011) Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming. Front. Plant Sci. 2: 39
Voll LM, Horst RJ, Zajic D, Voitsik AM, Engelsdorf T, Samans B, Pons-Kühnemann J, Hofmann J, Schmiedl A, Doehlemann G, Wahl R, Molitor A, Waller F, Kahmann R, Kämper J, Kogel KH, Sonnewald U
(See online at https://doi.org/10.3389/fpls.2011.00039) - (2011) Identification of virulence genes in the corn pathogen Colletotrichum graminicola by Agrobacterium tumefaciens-mediated transformation. Mol. Plant Pathol. 12: 43-55
Münch S, Ludwig N, Floß DS, Sugui JA, Koszucka AM, Voll LM, Sonnewald U, Deising HB
(See online at https://doi.org/10.1111/j.1364-3703.2010.00651.x) - (2011) Transcriptome and metabolite analysis of the barley-powdery mildew interaction reveals priming as a mechanism of P. indica-induced systemic resistance. MPMI, 24: 1427-39
Molitor A, Zajic D, Voll LM, Pons-Kühnemann J, Kogel KH, Waller F
(See online at https://doi.org/10.1094/MPMI-06-11-0177) - (2012) Indole derivatives production by the root endophyte Piriformospora indica is required for biotrophic colonization of barley but not for growth promotion. New Phytol. 196: 520-534
Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A
(See online at https://doi.org/10.1111/j.1469-8137.2012.04275.x) - (2012) Loss of cytosolic NADP-malic enzyme 2 in Arabidopsis is associated with enhanced susceptibility towards Colletotrichum higginsianum. New Phytol., 195: 189-202
Voll LM, Zell MB, Engelsdorf T, Saur A, Gerrard Wheeler M, Drincovich MF, Weber APM, Maurino VG
(See online at https://doi.org/10.1111/j.1469-8137.2012.04129.x) - (2012) The Ustilago maydis Nit2 homolog regulates nitrogen utilization and is required for efficient induction of filamentous growth. Eukaryot. Cell, 11:368-80
Horst RJ, Zeh C, Sonnewald S, Sonnewald U, Voll LM
(See online at https://doi.org/10.1128/EC.05191-11) - (2013) Reduced carbohydrate availability enhances susceptibility of Arabidopsis towards Colletotrichum higginsianum. Plant Physiol.
Engelsdorf T, Horst RJ, Pröls R, Pröschel M, Dietz CFD, Hückelhoven R, Voll LM
(See online at https://doi.org/10.1104/pp.112.209676)
