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Potentials, Utilization, and Bioengineering of Plant Growth-Promoting Methylobacterium for Sustainable Agriculture

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Potentials, Utilization, and Bioengineering of Plant Growth-Promoting Methylobacterium for Sustainable Agriculture sustainability Review Potentials, Utilization, and Bioengineering of Plant Growth-Promoting Methylobacterium for Sustainable Agriculture Cong Zhang 1,†, Meng-Ying Wang 1,†, Naeem Khan 2 , Ling-Ling Tan 1,* and Song Yang 1,3,* 1 School of Life Sciences, Shandong Province Key Laboratory of Applied Mycology, Qingdao Agricultural University, Qingdao 266000, China; [email protected] (C.Z.); [email protected] (M.-Y.W.) 2 Department of Agronomy, Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611, USA; naeemkhan@ufl.edu 3 Key Laboratory of Systems Bioengineering, Ministry of Education, Tianjin University, Tianjin 300000, China * Correspondence: [email protected] (L.-L.T.); [email protected] (S.Y.) † These authors equally contributed to this work. Abstract: Plant growth-promoting bacteria (PGPB) have great potential to provide economical and sustainable solutions to current agricultural challenges. The Methylobacteria which are frequently present in the phyllosphere can promote plant growth and development. The Methylobacterium genus is composed mostly of pink-pigmented facultative methylotrophic bacteria, utilizing organic one-carbon compounds as the sole carbon and energy source for growth. Methylobacterium spp. have been isolated from diverse environments, especially from the surface of plants, because they can oxidize and assimilate methanol released by plant leaves as a byproduct of pectin formation during cell wall synthesis. Members of the Methylobacterium genus are good candidates as PGPB Citation: Zhang, C.; Wang, M.-Y.; due to their positive impact on plant health and growth; they provide nutrients to plants, modulate Khan, N.; Tan, L.-L.; Yang, S. phytohormone levels, and protect plants against pathogens. In this paper, interactions between Potentials, Utilization, and Methylobacterium spp. and plants and how the bacteria promote crop growth is reviewed. Moreover, Bioengineering of Plant the following examples of how to engineer microbiomes of plants using plant-growth-promoting Growth-Promoting Methylobacterium for Sustainable Agriculture. Methylobacterium are discussed in the present review: introducing external Methylobacterium spp. Sustainability 2021, 13, 3941. https:// to plants, introducing functional genes or clusters to resident Methylobacterium spp. of crops, and doi.org/10.3390/su13073941 enhancing the abilities of Methylobacterium spp. to promote plant growth by random mutation, acclimation, and engineering. Academic Editor: Muhammad Naveed Keywords: Methylobacterium; biofertilizer; biostimulator; biocontrol; plant growth promoting bacte- ria; microbiome engineering Received: 19 February 2021 Accepted: 24 March 2021 Published: 02 April 2021 1. Introduction Publisher’s Note: MDPI stays neutral The population is increasing rapidly on Earth, reaching 7.8 billion and is estimated to with regard to jurisdictional claims in exceed 9 billion by 2050 (data according to the United Nations Department of Economic and published maps and institutional affil- Social Affairs). How to feed the increased population is a major challenge for agriculture. To iations. solve this problem, global food production needs to be increased by 70% to meet demands by 2050 [1]. Therefore, agriculture must be developed in a more sustainable and affordable way. In recent years, chemical fertilizers and pesticides have been used intensively to increase crop yields [2]. Neither chemical fertilizers nor chemical pesticides have been Copyright: © 2021 by the authors. found to be environmentally friendly or ecologically sustainable. Moreover, the application Licensee MDPI, Basel, Switzerland. of chemical fertilizers or pesticides always pollutes the surrounding water and air [3]. This article is an open access article Chemical fertilizers and pesticides may destroy the soil nutrient balance, lead to poor soil distributed under the terms and quality, and give rise to a variety of plant diseases [4,5]. Thus, substitutes for chemical conditions of the Creative Commons Attribution (CC BY) license (https:// fertilizers and pesticides are needed to increase crop yields in a sustainable way. Microbial creativecommons.org/licenses/by/ agents that promote plant growth and yield have the potential to be utilized in agriculture 4.0/). in the future. Sustainability 2021, 13, 3941. https://doi.org/10.3390/su13073941 https://www.mdpi.com/journal/sustainability Sustainability 2021, 13, x FOR PEER REVIEW 2 of 13 chemical fertilizers and pesticides are needed to increase crop yields in a sustainable way. Sustainability 2021, 13, 3941 2 of 12 Microbial agents that promote plant growth and yield have the potential to be utilized in agriculture in the future. PlantPlant microbiomes, microbiomes, which which incl includeude microbial microbial communities communities th thatat live, live, thrive, thrive, and and inter- inter- actact with with tissues tissues such such as as leaves, leaves, flowers, flowers, r roots,oots, shoots, shoots, and and seeds, seeds, could could improve improve growth, growth, health,health, and and production production of of plants plants and and protect protect plants plants from from potential potential pathogens pathogens [6]. [6]. Plant Plant microbiomesmicrobiomes are are composed composed of of bacteria, bacteria, fungi, fungi, and and archaea archaea [7,8], [7, 8among], among which which bacterial bacte- microbiomesrial microbiomes are regarded are regarded to play to important play important roles in roles promoting in promoting plant growth, plant growth, and could and becould used be in usedagriculture in agriculture as microbial as microbial agents (https://www.newleafsym agents (https://www.newleafsym.com/.com/ (accessed on (ac- 26 Marchcessed 2021 on 26)). MarchThe Methylobacterium 2021)). The Methylobacterium genus is one of genusthe major is one components of the major of plant components micro- biomes.of plant The microbiomes. diversity of The the diversityMethylobacterium of the Methylobacterium community in soilcommunity is influenced in soil by isplants influ- growthenced by[9]. plants The Methylobacterium growth [9]. The genusMethylobacterium was proposedgenus in 1976 was and proposed is composed in 1976 of Gram- and is negativecomposed bacteria of Gram-negative belonging to bacteria the α-proteobacteria belonging to the family.α-proteobacteria Bacteria of family.the Methylobacte- Bacteria of riumthe Methylobacteriumgenus generally havegenus pink generally pigmentation have pink due pigmentation to carotenoid due synthesis. to carotenoid They are synthe- able tosis. utilize They organic are able one-carbon to utilize organic compounds one-carbon (Figure compounds 1), such as (Figure formate,1), such formaldehyde, as formate, methanol,formaldehyde, and methylamine, methanol, and as methylamine,the sole carbon as and the soleenergy carbon source and for energy growing. source Most for membersgrowing. of Most the members Methylobacterium of the Methylobacterium genus are denotedgenus as are “pin denotedk-pigmented as “pink-pigmented facultative methylotrophs”facultative methylotrophs” (PPFM). (PPFM). FigureFigure 1. 1. MetabolicMetabolic modules modules of of α-proteobacteria-proteobacteria ( (AA)) and and γ-proteobacteria-proteobacteria ( (BB)) methylotrophs. methylotrophs. For For alpha-proteobacteria alpha-proteobacteria methylotrophs, it has three interlocked metabolic cycles, that is, the serine cycle, the ethylmalonyl-CoA (EMC) pathway, methylotrophs, it has three interlocked metabolic cycles, that is, the serine cycle, the ethylmalonyl-CoA (EMC) pathway, and the poly-3-hydroxybutyrate (PHB) cycle for C1 assimilation. The overlapped intermediates have been shown. For and the poly-3-hydroxybutyrate (PHB) cycle for C1 assimilation. The overlapped intermediates have been shown. For gamma-proteobacteria methylotrophs, the intermediate pyruvate generated from ribulose monophosphate (RuMP) path- waygamma-proteobacteria is decarboxylized into methylotrophs, acetyl-CoA, the which intermediate then enters pyruvate the tricarboxyl generatedic fromacid (TCA) ribulose cycle. monophosphate (RuMP) pathway is decarboxylized into acetyl-CoA, which then enters the tricarboxylic acid (TCA) cycle. To date, 60 species have been classified in the Methylobacterium genus To date, 60 species have been classified in the Methylobacterium genus (https://www. (https://www.bacterio.net/genus/methylobacterium (accessed on 26 March 2021)), and 11 bacterio.net/genus/methylobacterium (accessed on 26 March 2021)), and 11 species have species have been classified into a new genus, Methylorubrum. As all members of the been classified into a new genus, Methylorubrum. As all members of the Methylorubrum Methylorubrum genus belonged to the Methylobacterium genus before 2018, we discuss genus belonged to the Methylobacterium genus before 2018, we discuss them together them together as Methylobacterium spp. Some members of the Methylobacterium genus as Methylobacterium spp. Some members of the Methylobacterium genus dominate the dominate the phyllosphere for some plants, especially crops such as rice, clover, and soy- phyllosphere for some plants, especially crops such as rice, clover, and soybean [8]. For bean [8]. For example, the strains of M. extorquens PA1 and M. oryzae were isolated from example, the strains of M. extorquens PA1 and M. oryzae were isolated from the phyllo- the phyllosphere of Arabidopsis thaliana and rice [10,11]. Other members such as M. nodu- sphere of Arabidopsis thaliana
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