Signaling Components Shaping Arabidopsis Defense and Susceptibility in Nematode Interactions

Abstract

Plant-parasitic nematodes (PPNs) are roundworms distinguished by a spear-like stylet at the anterior end of their body, which they use to mechanically damage host cells and facilitate entry. This stylet also serves as a conduit for effectors, proteins that manipulate and modify host biology and it ultimately functions as a siphon to extract nutrients from the host after successful establishment. PPN-associated diseases result in substantial economic losses, estimated at over 150 billion USD annually. Given their economic significance, considerable research has focused on developing management strategies such as chemical treatments, the use of resistant and tolerant varieties, and cultural practices like flooding and crop rotation. However, current PPN management options have significant drawbacks, including the ecological harm caused by chemical controls and the breakdown of resistance in previously resistant crop cultivars. Therefore, there is a pressing need to further investigate the complex interactions between hosts and PPNs to gain mechanistic insights. Such understanding is crucial for developing novel, effective, and sustainable management solutions.<br /> <br /> This thesis therefore investigates two major axes of nematode defense, focusing on host susceptibility factors and molecular signaling mechanisms. First, we reveal that Ascaroside#18, a nematode-derived molecular pattern, triggers a unique leucine-rich repeat receptor NILR1-independent defence, distinct from classical pattern-triggered immunity (PTI). Unlike typical PTI, ascr#18-associated resistance acts without causing reactive oxygen species bursts or growth inhibition and operates independently of the peroxisomal β-oxidation pathway. Transcriptomic profiling shows that defense is mediated by downregulation of auxin transport and signaling genes, ultimately suppressing susceptibility to cyst nematodes without activating classical defense pathways. Reduced auxin influx carrier AUX1 and downstream auxin-responsive genes SAUR69 and IAA27 coincide with impaired nematode feeding cell development, highlighting the critical role of auxin signaling as a susceptibility factor.<br /> <br /> Secondly, work on heterotrimeric G-protein signaling delineates the role of extra-large G-proteins XLG2 and XLG3 as central susceptibility factors induced downstream of cytokinin (CK) signaling. These factors promote nematode parasitism, as demonstrated by Arabidopsis <em>xlg123</em> mutant lines showing reduced susceptibility to both cyst and root-knot nematode infection, with reduced nematode fitness and impaired feeding structures. XLG2 and XLG3 expression is shown to be CK-dependent, establishing a mechanistic link between hormone signaling and G-protein-mediated susceptibility pathways in host-pathogen interactions.<br /> <br /> Collectively, these findings underscore the importance of susceptibility factor modulation via auxin and cytokinin-linked signaling components in nematode defense. The thesis integrates novel insights into how plant immunity can be enhanced by reducing susceptibility, rather than by solely activating classical immune responses. This mechanistic knowledge opens new directions for crop engineering to achieve durable, broad-spectrum nematode resistance.