Browsing by Subject "Haustorium"

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Mobile signals in plant parasitism
(2024) Greifenhagen, Anne; Schaller, Andreas
Close to two percent of all flowering plants evolved parasitism, with some parasitic species, like Striga spp. from the Orobanchaceae family, posing a prevailing threat to crop yield. Parasitic weed management is challenging and requires a deeper understanding of the complex parasite-host relationship (Section 1.1). Parasitic plants infect and parasitize host plants through a multicellular feeding organ, the haustorium. This organ may either develop from the root tip as a single terminal haustorium or emerge multiple times along the growing roots, called lateral haustoria. In both cases, protohaustoria develop into mature haustoria that enable the withdrawal of water and nutrients. Parasitism depends on parasite and host endogenous signaling but also on communication between both partners (Section 1.2). This is similar to the development of other plant organs like lateral roots and symbiotic nodules, whose number is adjusted by an autoregulation of nodulation (AON) system. The induction of parasitic organs by pathogenic nematodes, but in particular also by parasitic plants, involves the manipulation, neofunctionalization, and interspecific exchange of mobile signals (Section 1.3). However, most of these molecular cues remain elusive in the parasitic plant-host plant interaction. This work aimed to address the biogenesis and function of parasite-derived endogenous and interspecific mobile signals involved in early till late stages of parasitism in the model system Phtheirospermum japonicum infecting Arabidopsis thaliana (Section 1.4). Transcriptome and genome studies on parasitic plants paved the way to unravel signaling cues contributing to parasitism. The evolution of parasitism correlates with the expansion of certain gene families followed by their parasitism-related neofunctionalization as seen for the KARRIKIN-INSENSITIVE 2 ‘divergent’-type (KAI2d) gene family in parasitic plants of the Orobanchaceae. Likewise, subtilisin-like serine protease (subtilase, SBT) genes in P. japonicum and Striga underwent an expansion, and some show haustorium tip-specific expression. The proteolytic activity of PjSBTs is required for proper haustorium formation and development. Despite their importance, no substrates of PjSBTs have been identified. In this work, PjSBT1.2.3 was found to be co-expressed with CLAVATA3(CLV)/EMBRYO-SURROUNDING REGION-related 3 (PjCLE3) during infection in the same domain of the haustorium. PjSBT1.2.3 cleaved PjCLE3 in vitro, thereby releasing the bioactive mature PjCLE3 peptide (Section 2.1, Fig.2.1.1). Sensing host-derived haustorium-inducing factors (HIFs) initiates haustorium organogenesis. In the absence of a host, the synthetic mature PjCLE3 induced protohaustorium formation similar to a host-derived benzoquinone HIF. Combined treatment of both HIFs potentiated their activity (Section 2.1, Fig.2.1.2). Pj cle3 knock-out hairy roots (HRs) formed fewer haustoria, particularly due to the absence of secondary protohaustoria (Section 2.1, Fig.2.1.3). These data demonstrate the existence of an autoregulation of haustoria formation (AOH) system as part of which the PjSBT1.2.3-PjCLE3 module, in analogy to AON, regulates the number of P. japonicum lateral haustoria. During the early stages of parasitism, the parasitism-related PjSBT1.2.3-PjCLE3 module promotes protohaustorium formation by sensitizing the parasite root for host-derived HIFs (Section 3.1). A homologous SBT-CLE module also exists in Striga, even though the parasite forms a terminal haustorium. Striga CLE2s are identical to host CLEs and this mimicry might improve nutrient allocations from the host during later stages of parasitism (Section 2.1, Fig.S2.1.2; Section 3.2). Similarly, parasite-derived cytokinin (CK) translocates through the haustorium inducing host hypertrophy, a swelling of host tissue above the infection site, thereby potentially benefiting parasite nutrient acquisition. In agrobacteria and plants, isopentenyltransferases (IPTs) synthesize CK precursors. Similar to SBTs and KAI2ds from parasitic plants, P. japonicum and S. hermonthica IPT1 genes exist as multiple copies, with one copy, PjIPT1a showing specific expression at the tip of haustoria (Section 2.2, Fig.2.2.1, Fig.2.2.2). Bioinformatic tools predicted a chloroplast transit peptide (CTP) for PjIPT1s, but PjIPT1-GFP fusions localized to cytoplasm and nucleus suggesting the CTP to be non-functional (Section 2.2, Fig.2.2.2, Fig.S2.2.2). To test substrate specificity and activity of both PjIPT1 copies, isoprenylation-activity was probed in vitro. PjIPT1b used both AMP and ATP as substrates, whereas PjIPT1a displayed a higher affinity for AMP, indicating that PjIPT1b may be the canonical, whereas PjIPT1a is the parasitism-related IPT (Section 2.2, Fig.2.2.4). This is further supported by the observation that CRISPR/Cas9-mediated mutation of PjIPT1a abolishes CK responses in the infected host (Section 3.3, Section 2.2, Fig.2.2.3). SBT-CLE, IPT-CK together with KAI2ds all have in common that their parasitism-related function may evolutionally result from gene duplication combined with neofunctionalization. Targeting duplicated and neofunctionalized genes may prove to be a promising strategy to combat parasitic weeds. (Sections 3.4, 3.5).