Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress

Abstract Saline–alkali stress is a severely adverse abiotic stress limiting plant growth. Malus halliana Koehne is an apple rootstock that is tolerant to saline–alkali stress. To understand the molecular mechanisms underlying the tolerance of M. halliana to saline–alkali stress, an integrated metabo...

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Main Authors: Xu-mei Jia, Yan-fang Zhu, Ya Hu, Rui Zhang, Li Cheng, Zu-lei Zhu, Tong Zhao, Xiayi Zhang, Yan-xiu Wang
Format: Article
Language:English
Published: Oxford University Press 2019-08-01
Series:Horticulture Research
Online Access:https://doi.org/10.1038/s41438-019-0172-0
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author Xu-mei Jia
Yan-fang Zhu
Ya Hu
Rui Zhang
Li Cheng
Zu-lei Zhu
Tong Zhao
Xiayi Zhang
Yan-xiu Wang
author_facet Xu-mei Jia
Yan-fang Zhu
Ya Hu
Rui Zhang
Li Cheng
Zu-lei Zhu
Tong Zhao
Xiayi Zhang
Yan-xiu Wang
author_sort Xu-mei Jia
collection DOAJ
description Abstract Saline–alkali stress is a severely adverse abiotic stress limiting plant growth. Malus halliana Koehne is an apple rootstock that is tolerant to saline–alkali stress. To understand the molecular mechanisms underlying the tolerance of M. halliana to saline–alkali stress, an integrated metabolomic and proteomic approach was used to analyze the plant pathways involved in the stress response of the plant and its regulatory mechanisms. A total of 179 differentially expressed proteins (DEPs) and 140 differentially expressed metabolites (DEMs) were identified. We found that two metabolite-related enzymes (PPD and PAO) were associated with senescence and involved in porphyrin and chlorophyll metabolism; six photosynthesis proteins (PSAH2, PSAK, PSBO2, PSBP1, and PSBQ2) were significantly upregulated, especially PSBO2, and could act as regulators of photosystem II (PSII) repair. Sucrose, acting as a signaling molecule, directly mediated the accumulation of D-phenylalanine, tryptophan, and alkaloid (vindoline and ecgonine) and the expression of proteins related to aspartate and glutamate (ASP3, ASN1, NIT4, and GLN1−1). These responses play a central role in maintaining osmotic balance and removing reactive oxygen species (ROS). In addition, sucrose signaling induced flavonoid biosynthesis by activating the expression of CYP75B1 to regulate the homeostasis of ROS and promoted auxin signaling by activating the expression of T31B5_170 to enhance the resistance of M. halliana to saline–alkali stress. The decrease in peroxidase superfamily protein (PER) and ALDH2C4 during lignin synthesis further triggered a plant saline–alkali response. Overall, this study provides an important starting point for improving saline–alkali tolerance in M. halliana via genetic engineering.
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spelling doaj.art-571b9ecf082e4663aed497cb3f10bb102022-12-22T02:39:40ZengOxford University PressHorticulture Research2052-72762019-08-016111910.1038/s41438-019-0172-0Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stressXu-mei Jia0Yan-fang Zhu1Ya Hu2Rui Zhang3Li Cheng4Zu-lei Zhu5Tong Zhao6Xiayi Zhang7Yan-xiu Wang8College of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityNorthwest Institute of Eco-Environment and Resources, Chinese Academy of ScienceCollege of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityCollege of Horticulture, Gansu Agricultural UniversityAbstract Saline–alkali stress is a severely adverse abiotic stress limiting plant growth. Malus halliana Koehne is an apple rootstock that is tolerant to saline–alkali stress. To understand the molecular mechanisms underlying the tolerance of M. halliana to saline–alkali stress, an integrated metabolomic and proteomic approach was used to analyze the plant pathways involved in the stress response of the plant and its regulatory mechanisms. A total of 179 differentially expressed proteins (DEPs) and 140 differentially expressed metabolites (DEMs) were identified. We found that two metabolite-related enzymes (PPD and PAO) were associated with senescence and involved in porphyrin and chlorophyll metabolism; six photosynthesis proteins (PSAH2, PSAK, PSBO2, PSBP1, and PSBQ2) were significantly upregulated, especially PSBO2, and could act as regulators of photosystem II (PSII) repair. Sucrose, acting as a signaling molecule, directly mediated the accumulation of D-phenylalanine, tryptophan, and alkaloid (vindoline and ecgonine) and the expression of proteins related to aspartate and glutamate (ASP3, ASN1, NIT4, and GLN1−1). These responses play a central role in maintaining osmotic balance and removing reactive oxygen species (ROS). In addition, sucrose signaling induced flavonoid biosynthesis by activating the expression of CYP75B1 to regulate the homeostasis of ROS and promoted auxin signaling by activating the expression of T31B5_170 to enhance the resistance of M. halliana to saline–alkali stress. The decrease in peroxidase superfamily protein (PER) and ALDH2C4 during lignin synthesis further triggered a plant saline–alkali response. Overall, this study provides an important starting point for improving saline–alkali tolerance in M. halliana via genetic engineering.https://doi.org/10.1038/s41438-019-0172-0
spellingShingle Xu-mei Jia
Yan-fang Zhu
Ya Hu
Rui Zhang
Li Cheng
Zu-lei Zhu
Tong Zhao
Xiayi Zhang
Yan-xiu Wang
Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
Horticulture Research
title Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
title_full Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
title_fullStr Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
title_full_unstemmed Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
title_short Integrated physiologic, proteomic, and metabolomic analyses of Malus halliana adaptation to saline–alkali stress
title_sort integrated physiologic proteomic and metabolomic analyses of malus halliana adaptation to saline alkali stress
url https://doi.org/10.1038/s41438-019-0172-0
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