Parasitic plant, from inside out: endophytic development inLathrophytum peckoltii(Balanophoraceae) in host liana roots from tribe Paullineae (Sapindaceae)

Abstract

Background and objectives Balanophoraceae is one of the most bizarre and biologically interesting plant clades. It groups species with peculiar features that offers an opportunity for investigating several aspects of parasite plant development and morphogenesis. We analyzed the development and the mature vegetative body of Lathrophytum. peckoltii Eichler, focusing on the formation of the host-parasite interface. Additionally, we analyzed how this parasitic interaction causes modifications to the anatomy of Paullinia uloptera Radlk and Serjania clematidifolia Cambess host roots. Methods Vegetative bodies of parasite at different developmental stages were collected while infesting the roots of Sapindaceae vines. Non-parasitized host roots were also collected for comparison. Light, epifluorescence, confocal, and scanning electron microscopy were used to analyze. Key results The vegetative axis’ initial cells divide repeatedly, originating a parenchymatous matrix, which occupies the space from the cortex to the vascular cylinder of the host’s root. In the matrix’s peripheral layers, located near the xylem of the host’s roots, a few cells initiate the process of wall lignification, originating parasitic bundle. The vascular cambium of the host’s root changes the division plane and becomes composed by fusiform initials, forming the vascular bundle. The vegetative axis presents a dermal tissue similar to a phellem, parenchymatous matrix and a vascular system with different origins. Conclusion The parasite reproduces by endophytic development, in a manner similar to that observed for endoparasites. The strategy of late cell differentiation could aid the parasite in avoiding early detection and triggering of defense responses by the host. This development causes changes to the host root cambial activity, leading to the establishment of direct, vessel-to-vessel connection between host and parasite. We associate these changes to the cambium modularity and an influx of parasite-derived hormones into the host cambium.

Vascular variants in seed plants—a developmental perspective

“…successive cambia in Cycas revoluta : Avetta 1887 ) and angiosperms ( Schenck 1893 ), including Nyctaginaceae ( Cunha Neto et al 2020b ) and Polygonaceae ( Rajput 2015 ), also with successive cambia, Bignoniaceae with phloem wedges ( Victorio 2016 ) or Apiaceae forming strands of vascular tissues called ‘multisteles’ ( Chuang 1970 ). Procambial variants in roots of seed plant lineages appear to be less common than those found in their respective stems, though the variants may be present in parasitic plants ( Kuijt and Bruns 1987 ; Carlquist 1988 ; Wilson and Calvin 1996 ; Pellissari et al . 2022 ).…”

Laser ablation tomography (LATscan) as a new tool for anatomical studies of woody plants

“…grafting), plant–pathogen associations, or parasitic plants‐host interactions, which normally requires complementary chemical analysis (e.g. histochemistry, fluorescence microscopy) to identify the tissues that are specific to the pathogen/parasitic plant or host plant, or to differentiate chemical compounds deposited in boundary layers of wounded plants (Rittinger et al ., 1987; Rath et al ., 2014; Navarro et al ., 2019; Pellissari et al ., 2022).…”

Laser ablation tomography (LATscan) as a new tool for anatomical studies of woody plants

“…Because LATscan enabled direct visualization of the spatial variation of some (lignin and suber) cell wall components without any chemical treatment or staining of cell walls, it can be considered another tool to facilitate the integration of histology and chemical analysis of cell walls in plants. In addition to gross anatomy, this approach may be particularly useful for studying complex systems such as wounding experiments (e.g., grafting), plant-pathogen associations or parasitic plants-host interactions, which normally requires complementary chemical analysis (e.g., histochemistry, fluorescence microscopy) to identify tissues that are specific to the pathogen/parasitic plant or host plant, or to differentiate chemical compounds deposited in boundary layers of wounded plants (Rittinger et al ., 1987; Rath et al ., 2014; Navarro et al ., 2019; Pellissari et al ., 2022).…”