PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana.

Reira Suzuki,Allen Yi-Lun Tsai,Mizuki Yamada,Mitsuhiro Aida,Minoru Kubo,Takumi Higaki,Shinichiro Sawa

doi:10.3389/fpls.2021.755610

Reira Suzuki, Allen Yi-Lun Tsai + Show 5 more

Open Access

https://doi.org/10.3389/fpls.2021.755610

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Abstract

Parasitic root-knot nematodes transform the host’s vascular cells into permanent feeding giant cells (GCs) to withdraw nutrients from the host plants. GCs are multinucleated metabolically active cells with distinctive cell wall structures; however, the genetic regulation of GC formation is largely unknown. In this study, the functions of the Arabidopsis thaliana transcription factor PUCHI during GC development were investigated. PUCHI expression was shown to be induced in early developing galls, suggesting the importance of the PUCHI gene in gall formation. Despite the puchi mutant not differing significantly from the wild type in nematode invasion and reproduction rates, puchi GC cell walls appeared to be thicker and lobate when compared to the wild type, while the cell membrane sometimes formed invaginations. In three-dimensional (3D) reconstructions of puchi GCs, they appeared to be more irregularly shaped than those in the wild type, with noticeable cell-surface protrusions and folds. Interestingly, the loss-of-function mutant of 3-KETOACYL-COA SYNTHASE 1 showed GC morphology and cell wall defects similar to those of the puchi mutant, suggesting that PUCHI may regulate GC development via very long chain fatty acid synthesis.

Highlights

Plant-parasitic nematodes, such as root-knot nematodes (RKNs, Meloidogyne spp.), are known to infect and damage a broad spectrum of crops
Quantitative reverse transcription polymerase chain-reaction results are consistent with the notion that Root-Knot Nematodes (RKNs) infection causes the accumulation of PUCHI transcripts, since PUCHI mRNA levels increased as gall formation progressed (Figure 1A)
GUS expression was observed mostly in the lateral root primordia (LRP) of uninfected roots, which is consistent with previous work (Figure 1B; Hirota et al, 2007)

Summary

Introduction

Plant-parasitic nematodes, such as root-knot nematodes (RKNs, Meloidogyne spp.), are known to infect and damage a broad spectrum of crops. RKNs feed on the vascular cells of host plant roots, which impedes plant development and may even lead to plant death. Infective RKN second instar (J2) larvae enter the host plant roots and migrate to the vasculature, where they induce the formation of special feeding sites called galls. It is thought that RKNs inject various effector proteins into vascular cells, which convert these cells into specialized feeding cells known as giant cells (GCs; Williamson and Gleason, 2003). Galls play an essential role in sustaining RKN development (Favery et al, 2016), and GCs form the majority of a gall’s volume and provide RKNs with nutrients. The development of PUCHI Regulates Giant Cell Morphology

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