The Parenchyma of Secondary Xylem and Its Critical Role in Tree Defense against Fungal Decay in Relation to the CODIT Model

Abstract

This review examines the roles that ray and axial parenchyma (RAP) plays against fungal pathogens in the secondary xylem of wood within the context of the CODIT model (Compartmentalization of Decay in Trees), a defense concept first conceived in the early 1970s by Alex Shigo. This model, simplistic in its design, shows how a large woody perennial is highly compartmented. Anatomical divisions in place at the time of infection or damage, (physical defense) alongside the ‘active’ response by the RAP during and after wounding work together in forming boundaries that function to restrict air or decay spread. The living parenchyma cells play a critical role in all of the four walls (differing anatomical constructs) that the model comprises. To understand how living cells in each of the walls of CODIT cooperate, we must have a clear vision of their complex interconnectivity from a three-dimensional perspective, along with knowledge of the huge variation in ray parenchyma (RP) and axial parenchyma (AP) abundance and patterns. Crucial patterns for defense encompass the symplastic continuum between both RP and AP and the dead tissues, with the latter including the vessel elements, libriform fibers, and imperforate tracheary elements (i.e., vasicentric and vascular tracheids). Also, the heartwood, a chemically altered antimicrobial non-living substance that forms the core of many trees, provides an integral part of the defense system. In the heartwood, dead RAP can play an important role in defense, depending on the genetic constitution of the species. Considering the array of functions that RAP are associated with, from capacitance, through to storage, and long-distance water transport, deciding how their role in defense fits into this suite of functions is a challenge for plant scientists, and likely depends on a range of factors. Here, we explore the important role of RAP in defense against fungal pathogens and the trade-offs involved from a viewpoint for structure-function relations, while also examining how fungi can breach the defense system using an array of enzymes in conjunction with the physically intrusive hyphae.

Bordered pits in xylem of vesselless angiosperms and their possible misinterpretation as perforation plates

“…; Morris et al . ), but at the same time may increase the hydraulic resistance (Sperry et al . ; Hacke et al .…”

“…Bordered pits on lateral walls provide the only direct pathway for water transport between neighbouring conduits (Sano et al 2011). One of the most important components of bordered pits include the pit membrane, which are traditionally assumed to prevent the spread of air and pathogens between conduits (Zimmermann & Brown 1971;Sperry & Tyree 1988;Choat et al 2008;Morris et al 2016), but at the same time may increase the hydraulic resistance Hacke et al 2006;Choat et al 2008). In conifer tracheids, the characteristic torus-margo pit membrane imposes much less hydraulic resistance than the homogeneous pit membrane in angiosperm vessels (Pittermann et al 2005;Choat et al 2008), because the pores in the margo can be >100 nm (Bouche et al 2014).…”

High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem

“…Xylem pit membranes are located in bordered pit pairs in conduit cell walls and develop from the primary cell wall and an intervening middle lamella of adjacent vessels (Jane, 1956;Sano, Morris, Shimada, & Jansen, 2011). Traditionally, pit membranes are assumed to serve as a capillary safety valve, because the nanoscale pore constrictions formed by the cellulose microfibrils in pit membranes may prevent the spreading of air and pathogens between vessels (Choat et al, 2008;Morris, Brodersen, Schwarze, & Jansen, 2016;Zimmermann, 1983;Zimmermann & Brown, 1971). Despite the importance of the pore constriction sizes and their highly variable shapes for the functioning of pit membranes, the ultrastructure of hydrated pit membranes has been explored in only few species (Pesacreta, Groom, & Rials, 2005).…”

Breeding and scientific advances in the fight against Dutch elm disease: Will they allow the use of elms in forest restoration?

“…The combination of chemical, physiological and anatomical defenses helps to compartmentalize the pathogen, while initial fungal contention results in greater capacity to maintain fungal restriction later on due to lower declines in sap flow, bark water content, photosynthesis and energy available to fuel secondary metabolism. In contrast, over-production of tyloses, gums and gels can be responsible for complete vessel blockage and hydraulic failure (Morris et al 2016). While the relationship of plant anatomical and chemical factors with DED resistance has been amply studied, the way these factors are related to each other and to plant physiology has received less attention.…”