Cargando…

Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies

Approximately one-third of agricultural land worldwide is affected by salinity, which limits the productivity and sustainability of crop ecosystems. Plant-growth-promoting rhizobacteria (PGPR) are a potential solution to this problem, as PGPR increases crop yield through improving soil fertility and...

Descripción completa

Detalles Bibliográficos
Autores principales: Shi, Lina, Zhu, Xiaoxia, Qian, Ting, Du, Jiazhou, Du, Yuanyuan, Ye, Jianren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10647267/
https://www.ncbi.nlm.nih.gov/pubmed/37958734
http://dx.doi.org/10.3390/ijms242115751
_version_ 1785135067103756288
author Shi, Lina
Zhu, Xiaoxia
Qian, Ting
Du, Jiazhou
Du, Yuanyuan
Ye, Jianren
author_facet Shi, Lina
Zhu, Xiaoxia
Qian, Ting
Du, Jiazhou
Du, Yuanyuan
Ye, Jianren
author_sort Shi, Lina
collection PubMed
description Approximately one-third of agricultural land worldwide is affected by salinity, which limits the productivity and sustainability of crop ecosystems. Plant-growth-promoting rhizobacteria (PGPR) are a potential solution to this problem, as PGPR increases crop yield through improving soil fertility and stress resistance. Previous studies have shown that Priestia megaterium ZS-3(ZS-3) can effectively help plants tolerate salinity stress. However, how ZS-3 regulates its metabolic adaptations in saline environments remains unclear. In this study, we monitored the metabolic rearrangement of compatibilisers in ZS-3 and combined the findings with genomic data to reveal how ZS-3 survives in stressful environments, induces plant growth, and tolerates stress. The results showed that ZS-3 tolerated salinity levels up to 9%. In addition, glutamate and trehalose help ZS-3 adapt to osmotic stress under low NaCl stress, whereas proline, K(+), and extracellular polysaccharides regulate the osmotic responses of ZS-3 exposed to high salt stress. Potting experiments showed that applying the ZS-3 strain in saline and neutral soils could effectively increase the activities of soil acid phosphatase, urease, and invertase in both soils, thus improving soil fertility and promoting plant growth. In addition, strain ZS-3-GFP colonised the rhizosphere and leaves of Cinnamomum camphora well, as confirmed by confocal microscopy and resistance plate count analysis. Genomic studies and in vitro experiments have shown that ZS-3 exhibits a variety of beneficial traits, including plant-promoting, antagonistic, and other related traits (such as resistance to saline and heavy metal stress/tolerance, amino acid synthesis and transport, volatile compound synthesis, micronutrient utilisation, and phytohormone biosynthesis/regulatory potential). The results support that ZS-3 can induce plant tolerance to abiotic stresses. These data provide important clues to further reveal the interactions between plants and microbiomes, as well as the mechanisms by which micro-organisms control plant health.
format Online
Article
Text
id pubmed-10647267
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-106472672023-10-30 Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies Shi, Lina Zhu, Xiaoxia Qian, Ting Du, Jiazhou Du, Yuanyuan Ye, Jianren Int J Mol Sci Article Approximately one-third of agricultural land worldwide is affected by salinity, which limits the productivity and sustainability of crop ecosystems. Plant-growth-promoting rhizobacteria (PGPR) are a potential solution to this problem, as PGPR increases crop yield through improving soil fertility and stress resistance. Previous studies have shown that Priestia megaterium ZS-3(ZS-3) can effectively help plants tolerate salinity stress. However, how ZS-3 regulates its metabolic adaptations in saline environments remains unclear. In this study, we monitored the metabolic rearrangement of compatibilisers in ZS-3 and combined the findings with genomic data to reveal how ZS-3 survives in stressful environments, induces plant growth, and tolerates stress. The results showed that ZS-3 tolerated salinity levels up to 9%. In addition, glutamate and trehalose help ZS-3 adapt to osmotic stress under low NaCl stress, whereas proline, K(+), and extracellular polysaccharides regulate the osmotic responses of ZS-3 exposed to high salt stress. Potting experiments showed that applying the ZS-3 strain in saline and neutral soils could effectively increase the activities of soil acid phosphatase, urease, and invertase in both soils, thus improving soil fertility and promoting plant growth. In addition, strain ZS-3-GFP colonised the rhizosphere and leaves of Cinnamomum camphora well, as confirmed by confocal microscopy and resistance plate count analysis. Genomic studies and in vitro experiments have shown that ZS-3 exhibits a variety of beneficial traits, including plant-promoting, antagonistic, and other related traits (such as resistance to saline and heavy metal stress/tolerance, amino acid synthesis and transport, volatile compound synthesis, micronutrient utilisation, and phytohormone biosynthesis/regulatory potential). The results support that ZS-3 can induce plant tolerance to abiotic stresses. These data provide important clues to further reveal the interactions between plants and microbiomes, as well as the mechanisms by which micro-organisms control plant health. MDPI 2023-10-30 /pmc/articles/PMC10647267/ /pubmed/37958734 http://dx.doi.org/10.3390/ijms242115751 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Shi, Lina
Zhu, Xiaoxia
Qian, Ting
Du, Jiazhou
Du, Yuanyuan
Ye, Jianren
Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title_full Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title_fullStr Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title_full_unstemmed Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title_short Mechanism of Salt Tolerance and Plant Growth Promotion in Priestia megaterium ZS-3 Revealed by Cellular Metabolism and Whole-Genome Studies
title_sort mechanism of salt tolerance and plant growth promotion in priestia megaterium zs-3 revealed by cellular metabolism and whole-genome studies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10647267/
https://www.ncbi.nlm.nih.gov/pubmed/37958734
http://dx.doi.org/10.3390/ijms242115751
work_keys_str_mv AT shilina mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies
AT zhuxiaoxia mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies
AT qianting mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies
AT dujiazhou mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies
AT duyuanyuan mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies
AT yejianren mechanismofsalttoleranceandplantgrowthpromotioninpriestiamegateriumzs3revealedbycellularmetabolismandwholegenomestudies