Root architecture plasticity in response to endoparasitic cyst nematodes is mediated by damage signaling

Abstract

Summary Plant root architecture plasticity in response to biotic stresses has not been thoroughly investigated. Infection by endoparasitic cyst nematodes induces root architectural changes that involve the formation of secondary roots at infection sites. However, the molecular mechanisms regulating secondary root formation in response to cyst nematode infection remain largely unknown. We first assessed whether secondary roots form in a nematode density‐dependent manner by challenging wild‐type Arabidopsis plants with increasing numbers of cyst nematodes (Heterodera schachtii). Next, using jasmonate‐related reporter lines and knockout mutants, we tested whether tissue damage by nematodes triggers jasmonate‐dependent secondary root formation. Finally, we verified whether damage‐induced secondary root formation depends on local auxin biosynthesis at nematode infection sites. Intracellular host invasion by H. schachtii triggers a transient local increase in jasmonates, which activates the expression of ERF109 in a COI1‐dependent manner. Knockout mutations in COI1 and ERF109 disrupt the nematode density‐dependent increase in secondary roots observed in wild‐type plants. Furthermore, ERF109 regulates secondary root formation upon H. schachtii infection via local auxin biosynthesis. Host invasion by H. schachtii triggers secondary root formation via the damage‐induced jasmonate‐dependent ERF109 pathway. This points at a novel mechanism underlying plant root plasticity in response to biotic stress.

WOX11-mediated cell size control in Arabidopsis attenuates fecundity of endoparasitic cyst nematodes

“…We recently reported that plant perception of cyst nematode invasion induces the formation of WOX11-adventitious lateral roots at nematode infection sites (Guarneri et al, 2023, Willig et al, 2023. Through this local root plasticity response, WOX11 compensates for the inhibition of primary root growth caused by nematode infection, which benefits overall plant growth and development (Willig et al, 2023). In this study, we shift perspective from the plant to the nematode and investigate whether WOX11-mediated developmental plasticity has an impact on nematode fecundity.…”

“…Thus, we concluded that WOX11 does not affect plant susceptibility to nematode infection but restricts nematode female fecundity in soil. The effect of WOX11 on syncytium hypertrophy and female fecundity is not causally linked to adventitious lateral root formation WOX11-adventitious lateral roots emerge in proximity or adjacent to nematode syncytia (Golinowski et al, 1996, Willig et al, 2023. As adventitious lateral roots are both strong sinks of assimilates (Stitz et al, 2023) and an additional source of water and minerals (Levin et al, 2020), we hypothesized that they could either compete or support syncytium hypertrophy and nematode fecundity.…”

“…Biotic stress by endoparasitic cyst nematodes disrupts plant growth by altering the flow of water and minerals through destructive migration within the roots and feeding (Trudgill et al, 1975, Grundler and Hofmann, 2011, Rodiuc et al, 2014, Levin et al, 2021. In response to nematode infection, plants trigger a damage signaling pathway mediated by WUSCHEL-RELATED HOMEOBOX11 (WOX11) that leads to the formation of adventitious lateral roots at nematode infection sites (Guarneri et al, 2023, Willig et al, 2023. WOX11-adventitious lateral roots compensate for the inhibition of primary root growth caused by cyst nematode infection and contribute to better maintenance of aboveground plant development and growth (Willig et al, 2023).…”

“…In response to nematode infection, plants trigger a damage signaling pathway mediated by WUSCHEL-RELATED HOMEOBOX11 (WOX11) that leads to the formation of adventitious lateral roots at nematode infection sites (Guarneri et al, 2023, Willig et al, 2023. WOX11-adventitious lateral roots compensate for the inhibition of primary root growth caused by cyst nematode infection and contribute to better maintenance of aboveground plant development and growth (Willig et al, 2023). Thus, WOX11 modulates plant tolerance to cyst nematode infections (Willig et al, 2023).…”

A Major Role of Class III HD-ZIPs in Promoting Sugar Beet Cyst Nematode Syncytium Formation inArabidopsis

“…Host genes related to auxin biosynthesis, distribution, and signaling are also modulated by CN at the infection site. YUCCA4 ( YUC4 ), encoding a member of YUCCA family enzymes that mediates a speed limiting step in the main auxin biosynthesis pathway, is up-regulated at the CN infection site, along with a few other auxin biosynthesis enzymes (Guarneri et al, 2022; Suzuki et al, 2022). Auxin efflux PIN1 and PIN7 genes are down-regulated at the early feeding site to prevent out flow of auxin from the initial syncytial cell, while PIN3 and PIN4 proteins are re-localized to the lateral membranes of the expanding syncytium to re-distribute auxin for lateral expansion of the syncytium (Grunewald et al, 2009).…”