Induced cell fate transitions at multiple cell layers configure haustorium development in parasitic plants

Abstract

The 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.

Subtilase activity in the intrusive cells mediates haustorium maturation in parasitic plants

“…Intrusive cells are derived from epidermal cells, but an epidermis marker construct ( pAtPGP4::3xVenus-NLS ) is not expressed in the intrusive region (Wakatake et al ., 2018). To further verify that ICSL1 expression is specific to intrusive cells, we used the ICSL1 promoter to drive a fluorescent marker module that localizes to the plasma membrane (3xmCherry-SYP; Wakatake et al ., 2018). In P. japoncium haustoria that were transformed with both pAtPGP4::3xVenus-NLS and pICSL1::3xmCherry-SYP , we found mutually exclusive expression patterns for the two constructs at 4 dpi (Supplemental Fig.…”

“…2A, C, E). This is the time point when expression of an epidermis marker ceases in the same region (Wakatake et al ., 2018). Thus, the developmental switch from epidermis to intrusive cell is likely to be activated around this time point.…”

“…All the Bpi I and Bsa I restriction sites within the cloned DNA sequences were mutated. The golden gate modules 3xVenus-NLS, 3xmCherry-SYP, pACT::3xmCherry-NLS , and pAtPGP4::3xVenus-NLS were described previously (Ishida et al ., 2016; Wakatake et al ., 2018).…”

“…In Orobanchaceae parasites, once the haustorium approaches the host, the epidermal cells in proximity to the host cells differentiate into intrusive cells, which have highly elongated shapes and function by intruding into the host (Musselman and Dickison, 1975). Once intrusive cells reach the host vasculature, some of the intrusive cells differentiate into xylem vessels, and subsequently formation of a xylem bridge (XB) between the parasite and host vasculature systems is initiated (Musselman and Dickison, 1975; Cui et al ., 2016; Wakatake et al ., 2018).…”

“…Among these was the auxin biosynthetic gene YUCCA3 , which contributes to auxin biosynthesis in the haustorium. This auxin undergoes intercellular transportation and leads to the differentiation of tracheary elements, resulting in the formation of the XB that connects the parasite with the host (Ishida et al ., 2016, Wakatake et al ., 2018; Wakatake et al ., 2020).…”