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

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 u...

Full description

Bibliographic Details
Main Authors: Reira Suzuki, Mizuki Yamada, Takumi Higaki, Mitsuhiro Aida, Minoru Kubo, Allen Yi-Lun Tsai, Shinichiro Sawa
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.755610/full
id doaj-d3868854f6d64765a41945c624113bb0
record_format Article
spelling doaj-d3868854f6d64765a41945c624113bb02021-10-06T07:26:25ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-10-011210.3389/fpls.2021.755610755610PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thalianaReira Suzuki0Mizuki Yamada1Takumi Higaki2Takumi Higaki3Mitsuhiro Aida4Mitsuhiro Aida5Minoru Kubo6Minoru Kubo7Allen Yi-Lun Tsai8Allen Yi-Lun Tsai9Shinichiro Sawa10Shinichiro Sawa11Department of Biological Sciences, Graduate School of Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Organization for Advanced Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Organization for Advanced Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Center for Agricultural and Environmental Biology, Kumamoto University, Kumamoto, JapanInternational Research Organization for Advanced Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Center for Agricultural and Environmental Biology, Kumamoto University, Kumamoto, JapanDepartment of Biological Sciences, Graduate School of Science and Technology, Kumamoto University, Kumamoto, JapanCenter for Digital Green-innovation, Nara Institute of Science and Technology, Nara, JapanDepartment of Biological Sciences, Graduate School of Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Center for Agricultural and Environmental Biology, Kumamoto University, Kumamoto, JapanDepartment of Biological Sciences, Graduate School of Science and Technology, Kumamoto University, Kumamoto, JapanInternational Research Center for Agricultural and Environmental Biology, Kumamoto University, Kumamoto, JapanParasitic 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.https://www.frontiersin.org/articles/10.3389/fpls.2021.755610/fullplant-parasitic nematodecell wallcell morphologyVLCFAplant-pathogen interaction
collection DOAJ
language English
format Article
sources DOAJ
author Reira Suzuki
Mizuki Yamada
Takumi Higaki
Takumi Higaki
Mitsuhiro Aida
Mitsuhiro Aida
Minoru Kubo
Minoru Kubo
Allen Yi-Lun Tsai
Allen Yi-Lun Tsai
Shinichiro Sawa
Shinichiro Sawa
spellingShingle Reira Suzuki
Mizuki Yamada
Takumi Higaki
Takumi Higaki
Mitsuhiro Aida
Mitsuhiro Aida
Minoru Kubo
Minoru Kubo
Allen Yi-Lun Tsai
Allen Yi-Lun Tsai
Shinichiro Sawa
Shinichiro Sawa
PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
Frontiers in Plant Science
plant-parasitic nematode
cell wall
cell morphology
VLCFA
plant-pathogen interaction
author_facet Reira Suzuki
Mizuki Yamada
Takumi Higaki
Takumi Higaki
Mitsuhiro Aida
Mitsuhiro Aida
Minoru Kubo
Minoru Kubo
Allen Yi-Lun Tsai
Allen Yi-Lun Tsai
Shinichiro Sawa
Shinichiro Sawa
author_sort Reira Suzuki
title PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
title_short PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
title_full PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
title_fullStr PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
title_full_unstemmed PUCHI Regulates Giant Cell Morphology During Root-Knot Nematode Infection in Arabidopsis thaliana
title_sort puchi regulates giant cell morphology during root-knot nematode infection in arabidopsis thaliana
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-10-01
description 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.
topic plant-parasitic nematode
cell wall
cell morphology
VLCFA
plant-pathogen interaction
url https://www.frontiersin.org/articles/10.3389/fpls.2021.755610/full
work_keys_str_mv AT reirasuzuki puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT mizukiyamada puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT takumihigaki puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT takumihigaki puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT mitsuhiroaida puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT mitsuhiroaida puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT minorukubo puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT minorukubo puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT allenyiluntsai puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT allenyiluntsai puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT shinichirosawa puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
AT shinichirosawa puchiregulatesgiantcellmorphologyduringrootknotnematodeinfectioninarabidopsisthaliana
_version_ 1716841257012035584