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A study on molecular mechanisms of haustorium development mediated by interspecies signaling between Cuscuta campestris and the host plant

Kaga Yuki 東北大学

2020.03.25

概要

During evolution of land plants, which originated as autotrophic organisms, some angiosperms have evolved parasitism. Currently, parasitic angiosperms account for more than 1% of angiosperm species. Typical parasitic plants parasitize either stems or roots of host plants via de novo formation of a distinctive parasitic organ called a haustorium, through which they absorb water and nutrients form the host plant.

All species of the genus Cuscuta, which lack proper roots and leaves, cannot survive without parasitizing the host plant. Instead they have evolved to be capable of developing haustoria in their stem, and can parasitize stem of a wide range of vascular plants. Thus Cuscuta species are classified as stem parasitic holoparasitic angiosperms. In the developing haustorium, meristematic cells, which are initiated from the cortex of the stem, differentiate into haustorial parenchyma cells, which elongate, penetrate into the host tissues and finally connect with the host vasculature. This interspecific vasculature connection allows the parasite to uptake water and nutrients from the host plant. Although histological aspects of haustorial development have been studied extensively, the molecular mechanisms underlying vasculature development and the interspecific connection with the host vasculature remain largely unknown.

In this study, I intended to reveal the molecular mechanisms regulating the haustorium development and subsequent interspecific connection with the host plant vasculature. Therefore, I investigated possible involvement of the interspecific cell-to- cell signaling between host plant and parasitic plant during the haustorium development of Cuscuta campestris. Time-course observation of the process of haustorium formation showed that xylem formation in the haustorium was initiated at haustorial tip cell, which had penetrated the host xylem, then proceeded basipetally, and eventually connected with the xylem in the Cuscuta lateral shoot. In the other organ of angiosperms, intercellular communication involving some phytohormones and ligand-receptor signaling pathways regulates vascular patterning, cell fate and cell differentiation. Based on my observations and the previous studies about vascular formation, I hypothesized that C. campestris receives host-derived signaling factors which trigger xylem vessel cell differentiation in haustorium upon intrusion of haustorium into host xylem, and initiates xylem formation in the parasitic organ.

Accordingly, to gain insights into the interspecific cell-to-cell interactions involved in haustorium development, I established an in vitro haustorium induction system for C. campestris using Arabidopsis thaliana rosette leaves as the host plant tissue. The in vitro induction system demonstrated that interactions with host tissue were required for the differentiation of parasite haustorial cells into xylem vessel cells. To further characterize the molecular events occurring during host-dependent xylem vessel cell differentiation in C. campestris, I performed a transcriptome analysis using samples from the in vitro induction system. The results showed that orthologs of genes involved in development and proliferation of vascular stem cells were up-regulated even in the absence of host tissue, whereas orthologs of genes required for xylem vessel cell differentiation were up- regulated only after some haustorial cells had elongated and intruded into the host xylem. This result was supported by another transcriptome analysis of the haustrorium development in C. campestris undergoing parasitization of a host plant. These findings suggest the involvement of host-derived signals in the regulation of non-autonomous xylem vessel differentiation and its connection to the host xylem during the haustorium development by activating a set of key genes for differentiation into xylem vessel cells.

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