Xylem vascular wilt pathogens cause devastating diseases in plants. Proliferation of these pathogens in the xylem causes massive disruption of water and mineral transport, resulting in severe wilting and death of the infected plants. Upon reaching the xylem vascular tissue, these pathogens multiply profusely, spreading vertically within the xylem sap, and horizontally between vessels and to the surrounding tissues. Plant resistance to these pathogens is very complex. One of the most effective defense responses in resistant plants is the formation of physico-chemical barriers in the xylem tissue. Vertical spread within the vessel lumen is restricted by structural barriers, namely, tyloses and gels. Horizontal spread to the apoplast and surrounding healthy vessels and tissues is prevented by vascular coating of the colonized vessels with lignin and suberin. Both vertical and horizontal barriers compartmentalize the pathogen at the infection site and contribute to their elimination. Induction of these defenses are tightly coordinated, both temporally and spatially, to avoid detrimental consequences such as cavitation and embolism. We discuss current knowledge on mechanisms underlying plant-inducible structural barriers against major xylem-colonizing pathogens. This knowledge may be applied to engineer metabolic pathways of vascular coating compounds in specific cells, to produce plants resistant towards xylem colonizers.

Summary: Tomato varieties resistant to the bacterial wilt pathogen Ralstonia solanacearum have the ability to restrict bacterial movement in the plant. Inducible vascular cell wall reinforcements seem to play a key role in confining R. solanacearum into the xylem vasculature of resistant tomato. However, the type of compounds involved in such vascular physico‐chemical barriers remain understudied, while being a key component of resistance. Here we use a combination of histological and live‐imaging techniques, together with spectroscopy and gene expression analysis to understand the nature of R. solanacearum‐induced formation of vascular coatings in resistant tomato. We describe that resistant tomato specifically responds to infection by assembling a vascular structural barrier formed by a ligno‐suberin coating and tyramine‐derived hydroxycinnamic acid amides. Further, we show that overexpressing genes of the ligno‐suberin pathway in a commercial susceptible variety of tomato restricts R. solanacearum movement inside the plant and slows disease progression, enhancing resistance to the pathogen. We propose that the induced barrier in resistant plants does not only restrict the movement of the pathogen, but may also prevent cell wall degradation by the pathogen and confer anti‐microbial properties, effectively contributing to resistance.

As a wall polymer, suberin has a multifaceted role in plant development and stress responses. It is deposited between the plasma membrane and the primary cell wall in specialized tissues such as root exodermis, endodermis, phellem, and seed coats. It is formed de novo in response to stresses such as wounding, salt injury, drought, and pathogen attack and is a complex polyester mainly consisting of fatty acids, glycerol, and minor amounts of ferulic acid that are associated to a lignin-like polymer predominantly composed of ferulates. Metabolomic and transcriptomic studies have revealed that cell wall lignification precedes suberin deposition. The ferulic acid esterified to ω-hydroxy fatty acids, synthetized by the feruloyl transferase FHT (or ASFT), presumably plays a role in coupling both polymers, although the precise mechanism is not understood. Here, we use the promoter of tomato suberin feruloyl transferase (FHT/ASFT) fused to GUS (β-glucuronidase) to demonstrate that ferulate deposition agrees with the site of promoter FHT activation by using a combination of histochemical staining and UV microscopy. Hence, FHT promoter activation and alkali UV microscopy can be used to identify the precise localization of early suberizing cells rich in ferulic acid and can additionally be used as an efficient marker of early suberization events during plant development and stress responses. This line can be used in the future as a tool to identify emerging suberization sites via ferulate deposition in tomato plants, which may contribute to germplasm screening in varietal improvement programs.