Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms

Soil salinity negatively modulates plant growth and development, contributing to severe decreases in the growth and production of crops. Mucilaginibacter sp. K is a root endophytic bacterium that was previously reported by our laboratory to stimulate growth and confer salt tolerance in Arabidopsis (...

Full description

Bibliographic Details
Main Authors: Di Fan, Donald L. Smith
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.938697/full
_version_ 1811334189690126336
author Di Fan
Di Fan
Donald L. Smith
author_facet Di Fan
Di Fan
Donald L. Smith
author_sort Di Fan
collection DOAJ
description Soil salinity negatively modulates plant growth and development, contributing to severe decreases in the growth and production of crops. Mucilaginibacter sp. K is a root endophytic bacterium that was previously reported by our laboratory to stimulate growth and confer salt tolerance in Arabidopsis (Arabidopsis thaliana). The main purpose of the present study is to elucidate the physiological and molecular machinery responsible for the prospective salt tolerance as imparted by Mucilaginibacter sp. K. We first report that auxin, gibberellin, and MPK6 signalings were required for strain K-induced growth promotion and salt tolerance in Arabidopsis. Then, this strain was assessed as a remediation strategy to improve maize performance under salinity stress. Under normal growth conditions, the seed vigor index, nitrogen content, and plant growth were significantly improved in maize. After NaCl exposure, strain K significantly promoted the growth of maize seedlings, ameliorated decline in chlorophyll content and reduced accretion of MDA and ROS compared with the control. The possible mechanisms involved in salt resistance in maize could be the improved activities of SOD and POD (antioxidative system) and SPS (sucrose biosynthesis), upregulated content of total soluble sugar and ABA, and reduced Na+ accumulation. These physiological changes were then confirmed by induced gene expression for ion transportation, photosynthesis, ABA biosynthesis, and carbon metabolism. In summary, these results suggest that strain K promotes plant growth through increases in photosynthesis and auxin- and MPK6-dependent pathways; it also bestows salt resistance on plants through protection against oxidative toxicity, Na+ imbalance, and osmotic stress, along with the activation of auxin-, gibberellin-, and MPK6-dependent signaling pathways. This is the first detailed report of maize growth promotion by a Mucilaginibacter sp. strain from wild plant. This strain could be used as a favorable biofertilizer and a salinity stress alleviator for maize, with further ascertainment as to its reliability of performance under field conditions and in the presence of salt stress.
first_indexed 2024-04-13T17:04:08Z
format Article
id doaj.art-5744d7dca93c42f4ab06492d7273d7d6
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-04-13T17:04:08Z
publishDate 2022-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-5744d7dca93c42f4ab06492d7273d7d62022-12-22T02:38:32ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-06-011310.3389/fpls.2022.938697938697Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel MechanismsDi Fan0Di Fan1Donald L. Smith2School of Biology, Food and Environment, Hefei University, Hefei, ChinaDepartment of Plant Science, McGill University, Montreal, QC, CanadaDepartment of Plant Science, McGill University, Montreal, QC, CanadaSoil salinity negatively modulates plant growth and development, contributing to severe decreases in the growth and production of crops. Mucilaginibacter sp. K is a root endophytic bacterium that was previously reported by our laboratory to stimulate growth and confer salt tolerance in Arabidopsis (Arabidopsis thaliana). The main purpose of the present study is to elucidate the physiological and molecular machinery responsible for the prospective salt tolerance as imparted by Mucilaginibacter sp. K. We first report that auxin, gibberellin, and MPK6 signalings were required for strain K-induced growth promotion and salt tolerance in Arabidopsis. Then, this strain was assessed as a remediation strategy to improve maize performance under salinity stress. Under normal growth conditions, the seed vigor index, nitrogen content, and plant growth were significantly improved in maize. After NaCl exposure, strain K significantly promoted the growth of maize seedlings, ameliorated decline in chlorophyll content and reduced accretion of MDA and ROS compared with the control. The possible mechanisms involved in salt resistance in maize could be the improved activities of SOD and POD (antioxidative system) and SPS (sucrose biosynthesis), upregulated content of total soluble sugar and ABA, and reduced Na+ accumulation. These physiological changes were then confirmed by induced gene expression for ion transportation, photosynthesis, ABA biosynthesis, and carbon metabolism. In summary, these results suggest that strain K promotes plant growth through increases in photosynthesis and auxin- and MPK6-dependent pathways; it also bestows salt resistance on plants through protection against oxidative toxicity, Na+ imbalance, and osmotic stress, along with the activation of auxin-, gibberellin-, and MPK6-dependent signaling pathways. This is the first detailed report of maize growth promotion by a Mucilaginibacter sp. strain from wild plant. This strain could be used as a favorable biofertilizer and a salinity stress alleviator for maize, with further ascertainment as to its reliability of performance under field conditions and in the presence of salt stress.https://www.frontiersin.org/articles/10.3389/fpls.2022.938697/fullMucilaginibacter sp.plant growth promotionsalt stressZea mays L.Arabidopsis
spellingShingle Di Fan
Di Fan
Donald L. Smith
Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
Frontiers in Plant Science
Mucilaginibacter sp.
plant growth promotion
salt stress
Zea mays L.
Arabidopsis
title Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
title_full Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
title_fullStr Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
title_full_unstemmed Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
title_short Mucilaginibacter sp. K Improves Growth and Induces Salt Tolerance in Nonhost Plants via Multilevel Mechanisms
title_sort mucilaginibacter sp k improves growth and induces salt tolerance in nonhost plants via multilevel mechanisms
topic Mucilaginibacter sp.
plant growth promotion
salt stress
Zea mays L.
Arabidopsis
url https://www.frontiersin.org/articles/10.3389/fpls.2022.938697/full
work_keys_str_mv AT difan mucilaginibacterspkimprovesgrowthandinducessalttoleranceinnonhostplantsviamultilevelmechanisms
AT difan mucilaginibacterspkimprovesgrowthandinducessalttoleranceinnonhostplantsviamultilevelmechanisms
AT donaldlsmith mucilaginibacterspkimprovesgrowthandinducessalttoleranceinnonhostplantsviamultilevelmechanisms