Abstract
ABSTRACTThe haustorium in parasitic plants is an organ specialized for invasion and nutrient uptake from host plant tissues. Despite its importance, the developmental processes of haustoria are mostly unknown. To understand the dynamics of cell fate change and cellular lineage during haustorium development, we performed live imaging-based marker expression analysis and cell-lineage tracing during haustorium formation in the model facultative root parasite Phtheirospermum japonicum. Our live-imaging analysis revealed that haustorium formation was associated with induction of simultaneous cell division in multiple cellular layers, such as epidermis, cortex and endodermis. In addition, we found that procambium-like cells, monitored by cell type-specific markers, emerged within the central region of the haustorium before xylem connection to the host plant. Our clonal analysis of cell lineages showed that cells in multiple cellular layers differentiated into procambium-like cells, whereas epidermal cells eventually transitioned into specialized cells interfacing with the host plant. Thus, our data provide a cell fate transition map during de novo haustorium organogenesis in parasitic plants.
Highlights
Parasitic plants independently evolved at least 12 times in angiosperms, and approximately 4500 parasitic species are known to date (Barkman et al, 2007; Westwood et al, 2010; Yoshida et al, 2016)
At the haustorium initiation site, cell division began nearly at the same time in different root cellular layers (Fig. 1C,I), with epidermal, cortex, endodermal cells exhibiting anticlinal initial division, and pericycle cells showing periclinal initial division (Fig. S1B,C). This is in stark contrast to other organ initiation processes in root, such as lateral root and nodule where anticlinal cell division in the pericycle initiates the organ development (Laskowski et al, 1995; Malamy and Benfey, 1997; Xiao et al, 2014)
As haustoria originate from relatively young tissues near the meristematic region compared to lateral root and nodule (Bhuvaneswari et al, 1980; Parizot et al, 2008), pericycle cells, which maintain stem cell activity in mature root tissue, and other cell types might retain the potential to divide upon haustorium induction
Summary
Parasitic plants independently evolved at least 12 times in angiosperms, and approximately 4500 parasitic species are known to date (Barkman et al, 2007; Westwood et al, 2010; Yoshida et al, 2016). Striga spp. and Orobanche spp. are devastating agricultural pests, infecting staple food crops (Parker, 2009; Spallek et al, 2013). The haustorium can be classified as lateral or terminal, depending on its developmental origin. The former develops laterally from the primary root of a facultative parasite, or from secondary roots of both facultative and obligate parasites. Terminal haustoria appear to have occurred with the subsequent independent evolution of obligate parasitism (Westwood et al, 2010)
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