Molecular Mechanisms of the 1-Aminocyclopropane-1-Carboxylic Acid (ACC) Deaminase Producing Trichoderma asperellum MAP1 in Enhancing Wheat Tolerance to Waterlogging Stress.

Mamoona Rauf,Humaira Gul,Kazim Ali,Muhammad Arif,Muhammad Hamayun,Muhammad Mizanur Rahman,Aziz Ud-Din,Muhammad Awais

doi:10.3389/fpls.2020.614971

Abstract

Waterlogging stress (WS) induces ethylene (ET) and polyamine (spermine, putrescine, and spermidine) production in plants, but their reprogramming is a decisive element for determining the fate of the plant upon waterlogging-induced stress. WS can be challenged by exploring symbiotic microbes that improve the plant’s ability to grow better and resist WS. The present study deals with identification and application of 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase-producing fungal endophyte Trichoderma asperellum (strain MAP1), isolated from the roots of Canna indica L., on wheat growth under WS. MAP1 positively affected wheat growth by secreting phytohormones/secondary metabolites, strengthening the plant’s antioxidant system and influencing the physiology through polyamine production and modulating gene expression. MAP1 inoculation promoted yield in comparison to non-endophyte inoculated waterlogged seedlings. Exogenously applied ethephon (ET synthesis inducer) and 1-aminocyclopropane carboxylic acid (ACC; ET precursor) showed a reduction in growth, compared to MAP1-inoculated waterlogged seedlings, while amino-oxyacetic acid (AOA; ET inhibitor) application reversed the negative effect imposed by ET and ACC, upon waterlogging treatment. A significant reduction in plant growth rate, chlorophyll content, and stomatal conductance was noticed, while H2O2, MDA production, and electrolyte leakage were increased in non-inoculated waterlogged seedlings. Moreover, in comparison to non-inoculated waterlogged wheat seedlings, MAP1-inoculated waterlogged wheat exhibited antioxidant–enzyme activities. In agreement with the physiological results, genes associated with the free polyamine (PA) biosynthesis were highly induced and PA content was abundant in MAP1-inoculated seedlings. Furthermore, ET biosynthesis/signaling gene expression was reduced upon MAP1 inoculation under WS. Briefly, MAP1 mitigated the adverse effect of WS in wheat, by reprogramming the PAs and ET biosynthesis, which leads to optimal stomatal conductance, increased photosynthesis, and membrane stability as well as reduced ET-induced leaf senescence.

Highlights

Waterlogging stress (WS) reduces the photosynthesis rate and induces oxidative stress
The present study revealed the potential of T. asperellum MAP1 to produce IAA, phenols, and flavonoids
MAP1 inoculation enhanced overall wheat growth in terms of higher chlorophyll content, accelerated growth rate, and increased stomatal conductance leading to higher biomass under normal as well as WS

Summary

Introduction

Waterlogging stress (WS) reduces the photosynthesis rate and induces oxidative stress. Wheat is one of the major cereals in Asia and is rather waterlogging-sensitive, flooding-tolerant relatives of Triticum have been reported such as Triticum macha L., Triticum dicoccum cv. Triticum aestivum L., a high-yielding and major cereal in Asia, is sensitive to waterlogged conditions. These conditions negatively affected shoot length, root/shoot dry weights, and leaf number of wheat seedlings (Yamauchi et al, 2018). Several fungi have the considerable ability to produce certain enzymes such as 1-aminocyclopropane-1-carboxylate-deaminase (ACC deaminase) produced by Trichoderma longibrachiatum T6 (TL-6) involved in promoting wheat (T. aestivum L.) growth and enhancing plant tolerance to NaCl stress (Zhang et al, 2019). Presence of ACC deaminase gene in the genome of species of Penicillium and Trichoderma triggered the modulation in the production of ET by the fungal

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