Invasion of the stigma by oomycete pathogenic hyphae or pollen tubes: striking similarities and differences

• Published in: Journal of experimental botany 2024-10, Vol.75 (20), p.6258-6274
• Main Authors: Riglet, Lucie, Hok, Sophie, Kebdani-Minet, Naïma, Le Berre, Joëlle, Gourgues, Mathieu, Rozier, Frédérique, Bayle, Vincent, Bancel-Vallée, Lesli, Allasia, Valérie, Keller, Harald, Da Rocha, Martine, Attard, Agnés, Fobis-Loisy, Isabelle
• Format: Article
• Language: English
• Subjects: Arabidopsis - microbiology; Arabidopsis - physiology; Flowers - microbiology; Flowers - physiology; Host-Pathogen Interactions; Hyphae - physiology; Life Sciences; Oomycetes - physiology; Plant Diseases - microbiology; Pollen Tube - growth & development; Pollen Tube - physiology
• ISSN: 0022-0957; 1460-2431; 1460-2431
• DOI: 10.1093/jxb/erae308

Abstract Both the pollen tube and hyphae of filamentous pathogens penetrate the outer layer of the host and then grow within host tissues. Early epidermal responses are decisive for the outcome of these two-cell interaction processes. We identified a single cell type, the papilla in the stigma of Arabidospis, as a tool to conduct a comprehensive comparative analysis on how an epidermal cell responds to the invasion of an unwanted pathogen or a welcome pollen tube. We showed that Phytophtora parasitica, a root oomycete, effectively breaches the stigmatic cell wall and develops as a biotroph within the papilla cytoplasm. These invasive features resemble the behaviour exhibited by the pathogen within its natural host cell, but diverge from the manner in which the pollen tube progresses, being engulfed within the papilla cell wall. Quantitative analysis revealed that both invaders trigger reorganization of the stigmatic endomembrane system and the actin cytoskeleton. While some remodelling processes are shared between the two interactions, others appear more specific towards the respective invader. These findings underscore the remarkable ability of an epidermal cell to differentiate between two types of invaders, thereby enabling it to trigger the most suitable response during the onset of invasion. Comparing how a stigmatic cell responds to a pathogen hypha or a pollen tube invasion reveals its remarkable ability to trigger specific sub-cellular features to orchestrate the most appropriated response.