Abstract

The interaction between the plant host, walnut (Juglans regia; Jr), and a deadly pathogen (Xanthomonas arboricola pv. juglandis 417; Xaj) can lead to walnut bacterial blight (WB), which depletes walnut productivity by degrading the nut quality. Here, we dissect this pathosystem using tandem mass tag quantitative proteomics. Walnut hull tissues inoculated with Xaj were compared to mock-inoculated tissues, and 3972 proteins were identified, of which 3296 are from Jr and 676 from Xaj. Proteins with differential abundance include oxidoreductases, proteases, and enzymes involved in energy metabolism and amino acid interconversion pathways. Defense responses and plant hormone biosynthesis were also increased. Xaj proteins detected in infected tissues demonstrate its ability to adapt to the host microenvironment, limiting iron availability, coping with copper toxicity, and maintaining energy and intermediary metabolism. Secreted proteases and extracellular secretion apparatus such as type IV pilus for twitching motility and type III secretion effectors indicate putative factors recognized by the host. Taken together, these results suggest intense degradation processes, oxidative stress, and general arrest of the biosynthetic metabolism in infected nuts. Our results provide insights into molecular mechanisms and highlight potential molecular tools for early detection and disease control strategies.

Highlights

  • Walnut (Juglans regia) is an economically important specialty crop, providing edible nuts, high-quality wood, and medicinal uses, with a distribution ranging from tropical to temperate zones in Asia, Europe, and the Americas [1,2,3]

  • An increased abundance of germin-like proteins (GLPs) in Walnut bacterial blight (WB) could be contributing to increased basal defense mechanisms, which are conserved in many plants and involve enzymatic activities like superoxide dismutase (SOD), oxalate oxidase, and polyphenol oxidase (PPO) [42]

  • The first proteome study of Jr infected with Xanthomonas arboricola pv. juglandis (Xaj), a high genetic diversity group among Xanthomonas, provided insights into the disease development in this pathosystem

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Summary

Introduction

Walnut (Juglans regia) is an economically important specialty crop, providing edible nuts, high-quality wood, and medicinal uses, with a distribution ranging from tropical to temperate zones in Asia, Europe, and the Americas [1,2,3]. It is among the most-produced nuts in the world, together with almonds, hazelnuts, pistachios, and cashews [4]. The biology of the host-pathogen interactions and the underlying molecular mechanisms that mediate the virulence, increased susceptibility, and/or resistance of the host plant have not been characterized This lack of knowledge leads to broad-spectrum and ineffective measures of disease control in the field. An increasing resistance to copper-based biocides in natural Xaj populations and an increasing dependence on EDBC fungicides for control trigger both immediate and long-term concerns regarding the viability of the continued registration of these compounds, due to their accumulation in the environment and toxicity [22]

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