Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants

Abscisic acid (ABA) is a critical phytohormone involved in multifaceted processes in plant metabolism and growth under both stressed and nonstressed conditions. Its accumulation in various tissues and cells has long been established as a biomarker for plant stress responses. To date, a comprehensive...

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Main Authors: Yuzhu Wang, Yeling Zhou, Jiansheng Liang
Format: Article
Language:English
Published: MDPI AG 2022-06-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/11/13/2039
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author Yuzhu Wang
Yeling Zhou
Jiansheng Liang
author_facet Yuzhu Wang
Yeling Zhou
Jiansheng Liang
author_sort Yuzhu Wang
collection DOAJ
description Abscisic acid (ABA) is a critical phytohormone involved in multifaceted processes in plant metabolism and growth under both stressed and nonstressed conditions. Its accumulation in various tissues and cells has long been established as a biomarker for plant stress responses. To date, a comprehensive understanding of ABA distribution and dynamics at subcellular resolution in response to environmental cues is still lacking. Here, we modified the previously developed ABA sensor ABAleon2.1_Tao3 (Tao3) and targeted it to different organelles including the endoplasmic reticulum (ER), chloroplast/plastid, and nucleus through the addition of corresponding signal peptides. Together with the cytosolic Tao3, we show distinct ABA distribution patterns in different tobacco cells with the chloroplast showing a lower level of ABA in both cell types. In a tobacco mesophyll cell, organellar ABA displayed specific alterations depending on osmotic stimulus, with ABA levels being generally enhanced under a lower and higher concentration of salt and mannitol treatment, respectively. In Arabidopsis roots, cells from both the meristem and elongation zone accumulated ABA considerably in the cytoplasm upon mannitol treatment, while the plastid and nuclear ABA was generally reduced dependent upon specific cell types. In Arabidopsis leaf tissue, subcellular ABA seemed to be less responsive when stressed, with notable increases of ER ABA in epidermal cells and a reduction of nuclear ABA in guard cells. Together, our results present a detailed characterization of stimulus-dependent cell type-specific organellar ABA responses in tobacco and Arabidopsis plants, supporting a highly coordinated regulatory network for mediating subcellular ABA homeostasis during plant adaptation processes.
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spelling doaj.art-ccc9891486c44586b55190de9d5d0ab52023-11-23T19:48:29ZengMDPI AGCells2073-44092022-06-011113203910.3390/cells11132039Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis PlantsYuzhu Wang0Yeling Zhou1Jiansheng Liang2Co-Innovation Center for Modern Production Technology of Grain Crops/Jiangsu Key Laboratory of Crop Genetics and Physiology, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Yangzhou University, Yangzhou 225009, ChinaKey Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen 518055, ChinaKey Laboratory of Molecular Design for Plant Cell Factory of Guangdong Higher Education Institutes, Department of Biology, School of Life Sciences, Southern University of Science and Technology, Shenzhen 518055, ChinaAbscisic acid (ABA) is a critical phytohormone involved in multifaceted processes in plant metabolism and growth under both stressed and nonstressed conditions. Its accumulation in various tissues and cells has long been established as a biomarker for plant stress responses. To date, a comprehensive understanding of ABA distribution and dynamics at subcellular resolution in response to environmental cues is still lacking. Here, we modified the previously developed ABA sensor ABAleon2.1_Tao3 (Tao3) and targeted it to different organelles including the endoplasmic reticulum (ER), chloroplast/plastid, and nucleus through the addition of corresponding signal peptides. Together with the cytosolic Tao3, we show distinct ABA distribution patterns in different tobacco cells with the chloroplast showing a lower level of ABA in both cell types. In a tobacco mesophyll cell, organellar ABA displayed specific alterations depending on osmotic stimulus, with ABA levels being generally enhanced under a lower and higher concentration of salt and mannitol treatment, respectively. In Arabidopsis roots, cells from both the meristem and elongation zone accumulated ABA considerably in the cytoplasm upon mannitol treatment, while the plastid and nuclear ABA was generally reduced dependent upon specific cell types. In Arabidopsis leaf tissue, subcellular ABA seemed to be less responsive when stressed, with notable increases of ER ABA in epidermal cells and a reduction of nuclear ABA in guard cells. Together, our results present a detailed characterization of stimulus-dependent cell type-specific organellar ABA responses in tobacco and Arabidopsis plants, supporting a highly coordinated regulatory network for mediating subcellular ABA homeostasis during plant adaptation processes.https://www.mdpi.com/2073-4409/11/13/2039abscisic acidFRET-FLIMsensororganellar-specificenvironmental stress
spellingShingle Yuzhu Wang
Yeling Zhou
Jiansheng Liang
Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
Cells
abscisic acid
FRET-FLIM
sensor
organellar-specific
environmental stress
title Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
title_full Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
title_fullStr Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
title_full_unstemmed Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
title_short Characterization of Organellar-Specific ABA Responses during Environmental Stresses in Tobacco Cells and Arabidopsis Plants
title_sort characterization of organellar specific aba responses during environmental stresses in tobacco cells and arabidopsis plants
topic abscisic acid
FRET-FLIM
sensor
organellar-specific
environmental stress
url https://www.mdpi.com/2073-4409/11/13/2039
work_keys_str_mv AT yuzhuwang characterizationoforganellarspecificabaresponsesduringenvironmentalstressesintobaccocellsandarabidopsisplants
AT yelingzhou characterizationoforganellarspecificabaresponsesduringenvironmentalstressesintobaccocellsandarabidopsisplants
AT jianshengliang characterizationoforganellarspecificabaresponsesduringenvironmentalstressesintobaccocellsandarabidopsisplants