TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots

The mitochondrial pyruvate dehydrogenase complex (PDC) plays a crucial role in linking the glycolysis pathway and the tricarboxylic acid (TCA) cycle. Previously, we reported that a mutation of MAB1, encoding an E1β subunit of PDC, affects the abundance of auxin efflux carriers PIN-FORMED proteins (P...

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Main Authors: Xiaomin Song, Iwai Ohbayashi, Song Sun, Qiuli Wang, Yi Yang, Mengyuan Lu, Yuanyuan Liu, Shinichiro Sawa, Masahiko Furutani
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-12-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1462235/full
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author Xiaomin Song
Xiaomin Song
Iwai Ohbayashi
Iwai Ohbayashi
Iwai Ohbayashi
Song Sun
Qiuli Wang
Qiuli Wang
Yi Yang
Yi Yang
Mengyuan Lu
Mengyuan Lu
Yuanyuan Liu
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
author_facet Xiaomin Song
Xiaomin Song
Iwai Ohbayashi
Iwai Ohbayashi
Iwai Ohbayashi
Song Sun
Qiuli Wang
Qiuli Wang
Yi Yang
Yi Yang
Mengyuan Lu
Mengyuan Lu
Yuanyuan Liu
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
author_sort Xiaomin Song
collection DOAJ
description The mitochondrial pyruvate dehydrogenase complex (PDC) plays a crucial role in linking the glycolysis pathway and the tricarboxylic acid (TCA) cycle. Previously, we reported that a mutation of MAB1, encoding an E1β subunit of PDC, affects the abundance of auxin efflux carriers PIN-FORMED proteins (PINs) via reduced recycling and enhanced degradation in vacuoles. Here, we further analyzed the effects of TCA cycle inhibition on vesicle trafficking using both the mab1-1 mutant and 3-BP, a TCA cycle inhibitor. Pharmacological and genetic impairment of the TCA cycle induced the aggregated components of ARA6, which is a plant-unique RAB5 GTPase that mediates endosomal trafficking to the plasma membrane. In addition, MAB4, which is an NPH3-like protein that inhibits PIN internalization from the plasma membrane, was severely reduced in 3-BP-treated roots and mab1-1. Furthermore, TCA cycle impairment led to the accumulation of reactive oxygen species in root tips, and treatment with H2O2 reduced MAB4 levels while increasing the internalization of PIN2 from the plasma membrane, and aggregated ARA6-positive compartments. These results suggest that TCA cycle impairment targets PIN proteins for degradation in the vacuole by disrupting both the MAB4-mediated block of internalization and the ARA6-mediated endocytic pathway.
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spelling doaj-art-d54acfb81dc94a2786c72b2c00e8f6072024-12-16T04:18:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2024-12-011510.3389/fpls.2024.14622351462235TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis rootsXiaomin Song0Xiaomin Song1Iwai Ohbayashi2Iwai Ohbayashi3Iwai Ohbayashi4Song Sun5Qiuli Wang6Qiuli Wang7Yi Yang8Yi Yang9Mengyuan Lu10Mengyuan Lu11Yuanyuan Liu12Shinichiro Sawa13Shinichiro Sawa14Shinichiro Sawa15Shinichiro Sawa16Masahiko Furutani17Masahiko Furutani18Masahiko Furutani19Masahiko Furutani20Masahiko Furutani21College of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaCollege of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaDepartment of Life Sciences, National Cheng Kung University, Tainan, TaiwanHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaCollege of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaCollege of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaCollege of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, Fujian Agriculture and Forestry University, Fujian, ChinaInstitute of Industrial Nanomaterial (IINA), Kumamoto University, Kumamoto, JapanInternational Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, JapanInternational Research Center for Agricultural and Environmental Biology (IRCAEB), Kumamoto University, Kumamoto, JapanGraduate School of Sciences and Technology, Kumamoto University, Kumamoto, JapanCollege of Life Sciences, Fujian Agriculture and Forestry University, Fujian, ChinaHaixia Institute of Science and Technology, Fujian Agriculture and Forestry University, Fujian, ChinaInstitute of Industrial Nanomaterial (IINA), Kumamoto University, Kumamoto, JapanInternational Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kumamoto, JapanDepartment of Earth System Science, Faculty of Science, Fukuoka University, Fukuoka, JapanThe mitochondrial pyruvate dehydrogenase complex (PDC) plays a crucial role in linking the glycolysis pathway and the tricarboxylic acid (TCA) cycle. Previously, we reported that a mutation of MAB1, encoding an E1β subunit of PDC, affects the abundance of auxin efflux carriers PIN-FORMED proteins (PINs) via reduced recycling and enhanced degradation in vacuoles. Here, we further analyzed the effects of TCA cycle inhibition on vesicle trafficking using both the mab1-1 mutant and 3-BP, a TCA cycle inhibitor. Pharmacological and genetic impairment of the TCA cycle induced the aggregated components of ARA6, which is a plant-unique RAB5 GTPase that mediates endosomal trafficking to the plasma membrane. In addition, MAB4, which is an NPH3-like protein that inhibits PIN internalization from the plasma membrane, was severely reduced in 3-BP-treated roots and mab1-1. Furthermore, TCA cycle impairment led to the accumulation of reactive oxygen species in root tips, and treatment with H2O2 reduced MAB4 levels while increasing the internalization of PIN2 from the plasma membrane, and aggregated ARA6-positive compartments. These results suggest that TCA cycle impairment targets PIN proteins for degradation in the vacuole by disrupting both the MAB4-mediated block of internalization and the ARA6-mediated endocytic pathway.https://www.frontiersin.org/articles/10.3389/fpls.2024.1462235/fullTCA cyclemtPDCauxin transportPINNPH3-likeROS
spellingShingle Xiaomin Song
Xiaomin Song
Iwai Ohbayashi
Iwai Ohbayashi
Iwai Ohbayashi
Song Sun
Qiuli Wang
Qiuli Wang
Yi Yang
Yi Yang
Mengyuan Lu
Mengyuan Lu
Yuanyuan Liu
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Shinichiro Sawa
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
Masahiko Furutani
TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
Frontiers in Plant Science
TCA cycle
mtPDC
auxin transport
PIN
NPH3-like
ROS
title TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
title_full TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
title_fullStr TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
title_full_unstemmed TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
title_short TCA cycle impairment leads to PIN2 internalization and degradation via reduced MAB4 level and ARA6 components in Arabidopsis roots
title_sort tca cycle impairment leads to pin2 internalization and degradation via reduced mab4 level and ara6 components in arabidopsis roots
topic TCA cycle
mtPDC
auxin transport
PIN
NPH3-like
ROS
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1462235/full
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