WOX11-mediated adventitious lateral root formation modulates tolerance of Arabidopsis to cyst nematode infections

Abstract

The transcription factor WUSCHEL-RELATED HOMEOBOX 11 (WOX11) in Arabidopsis initiates the formation of adventitious lateral roots upon mechanical injury in primary roots. Root-invading nematodes also induce de novo root organogenesis leading to excessive root branching, but it is not known if this symptom of disease involves mediation by WOX11 and if it benefits the plant. Here, we show with targeted transcriptional repression and reporter gene analyses in Arabidopsis that the beet cyst nematode Heterodera schachtii activates WOX11-adventitious lateral rooting from primary roots close to infection sites. The activation of WOX11 in nematode-infected roots occurs downstream of jasmonic acid-dependent damage signaling via ETHYLENE RESPONSIVE FACTOR109, linking adventitious lateral root formation to nematode damage to host tissues. By measuring different root system components, we found that WOX11-mediated formation of adventitious lateral roots compensates for nematode-induced inhibition of primary root growth. Our observations further demonstrate that WOX11-mediated rooting reduces the impact of nematode infections on aboveground plant development and growth. Altogether, we conclude that the transcriptional regulation by WOX11 modulates root system plasticity under biotic stress, which is one of the key mechanisms underlying tolerance of Arabidopsis to cyst nematode infections.

A matter of perspective : Root adaptive responses to endoparasitic cystnematodes

“…In a previous study, we showed that WOX11 modulates plant tolerance to infections by endoparasitic cyst nematodes (Willig et al, 2023a). Here, we asked whether this also affects nematode parasitism.…”

“…At this stage, syncytial elements are symplastically isolated from the surrounding host tissue, which likely enables the build op of turgor pressure required for cellular hypertrophy (Ruan et al, 2004;Hofmann et al, 2007). Since we previously observed that WOX11 and LBD16 are expressed between 2 and 7 dpi (Willig et al, 2023a), we asked whether WOX11 and LBD16 play a role in the early phases of syncytium expansion. To this end, we measured syncytium width in 35S::WOX11-SRDX and lbd16-2 mutants at 5 dpi.…”

“…WOX11-adventitious lateral roots emerge in proximity or adjacent to nematode syncytia (Golinowski et al, 1996;Willig et al, 2023a). 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 Willig et al, 2023a). 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, 2023a).…”

“…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 Willig et al, 2023a). 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, 2023a). Thus, WOX11 modulates plant tolerance to cyst nematode infections.…”