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Harnessing Bacterial Endophytes for Promotion of Plant Growth and Biotechnological Applications: an Overview

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Harnessing Bacterial Endophytes for Promotion of Plant Growth and Biotechnological Applications: an Overview plants Review Harnessing Bacterial Endophytes for Promotion of Plant Growth and Biotechnological Applications: An Overview Ahmed M. Eid 1 , Amr Fouda 1,* , Mohamed Ali Abdel-Rahman 1 , Salem S. Salem 1 , Albaraa Elsaied 1, Ralf Oelmüller 2, Mohamed Hijri 3,4 , Arnab Bhowmik 5 , Amr Elkelish 2,6 and Saad El-Din Hassan 1,* 1 Department of Botany and Microbiology, Faculty of Science, Al-Azhar University, Nasr City, Cairo 11884, Egypt; [email protected] (A.M.E.); [email protected] (M.A.A.-R.); [email protected] (S.S.S.); [email protected] (A.E.) 2 Department of Plant Physiology, Matthias Schleiden Institute of Genetics, Bioinformatics and Molecular Botany, Friedrich-Schiller-University, 07743 Jena, Germany; [email protected] (R.O.); [email protected] (A.E.) 3 Biodiversity Centre, Institut de Recherche en Biologie Végétale, Université de Montréal and Jardin botanique de Montréal, Montréal, QC 22001, Canada; [email protected] 4 African Genome Center, Mohammed VI Polytechnic University (UM6P), 43150 Ben Guerir, Morocco 5 Department of Natural Resources and Environmental Design, North Carolina A&T State University, Greensboro, NC 27411, USA; [email protected] 6 Botany Department, Faculty of Science, Suez Canal University, Ismailia 41522, Egypt * Correspondence: [email protected] (A.F.); [email protected] (S.E.-D.H.); Tel.: +20-1113-351-244 (A.F.); +20-1023-884-804 (S.E.-D.H.) Abstract: Endophytic bacteria colonize plants and live inside them for part of or throughout their Citation: Eid, A.M.; Fouda, A.; life without causing any harm or disease to their hosts. The symbiotic relationship improves the Abdel-Rahman, M.A.; Salem, S.S.; physiology, fitness, and metabolite profile of the plants, while the plants provide food and shelter Elsaied, A.; Oelmüller, R.; Hijri, M.; for the bacteria. The bacteria-induced alterations of the plants offer many possibilities for biotechno- Bhowmik, A.; Elkelish, A.; Hassan, logical, medicinal, and agricultural applications. The endophytes promote plant growth and fitness S.E.-D. Harnessing Bacterial through the production of phytohormones or biofertilizers, or by alleviating abiotic and biotic stress Endophytes for Promotion of Plant tolerance. Strengthening of the plant immune system and suppression of disease are associated Growth and Biotechnological Applications: An Overview. Plants with the production of novel antibiotics, secondary metabolites, siderophores, and fertilizers such as 2021, 10, 935. https://doi.org/ nitrogenous or other industrially interesting chemical compounds. Endophytic bacteria can be used 10.3390/plants10050935 for phytoremediation of environmental pollutants or the control of fungal diseases by the production of lytic enzymes such as chitinases and cellulases, and their huge host range allows a broad spectrum Academic Editor: Bertrand Hirel of applications to agriculturally and pharmaceutically interesting plant species. More recently, endo- phytic bacteria have also been used to produce nanoparticles for medical and industrial applications. Received: 11 April 2021 This review highlights the biotechnological possibilities for bacterial endophyte applications and Accepted: 3 May 2021 proposes future goals for their application. Published: 7 May 2021 Keywords: biotechnological applications; endophytes; plant growth; biofertilizers; phytohor- Publisher’s Note: MDPI stays neutral mones; phytoremediation with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Endophytes are fungal and bacterial organisms that inhabit the plant endosphere without harming their hosts. They live asymptomatically in the plant cellular environment Copyright: © 2021 by the authors. and perform symbiosis-specific functions such as synthesis of secondary metabolites or Licensee MDPI, Basel, Switzerland. signaling molecules that function as internal and external stimuli during the mutualistic This article is an open access article distributed under the terms and interaction [1]. Endophytic microbes are sources of novel biomolecules for the biochemical conditions of the Creative Commons and pharmaceutical industries [2]. They produce biologically active metabolites, including Attribution (CC BY) license (https:// immune-suppressive compounds, anticancer agents, plant growth promotors, antimi- creativecommons.org/licenses/by/ crobial volatiles, insecticides, antioxidants, and antibiotics [3,4], with huge potential for 4.0/). Plants 2021, 10, 935. https://doi.org/10.3390/plants10050935 https://www.mdpi.com/journal/plants Plants 2021, 10, x FOR PEER REVIEW 2 of 34 Plants 2021, 10, 935 2 of 33 for application in medicine, pharmaceutics industry, or agriculture (Figure 1). Moreover, endophyticapplication microbes in medicine, can pharmaceutics improve plant industry, growth under or agriculture harsh conditions (Figure1). such Moreover, as nutrient endo- stress,phytic temperature microbes can stress, improve salinit planty, trace growth metal under stress, harsh or conditions drought [5]. such They as nutrientcan also stress, help plantstemperature to grow stress, in contaminated salinity, trace environm metal stress,ents orby drought degrading [5]. hazardous They can also compounds. help plants We to describegrow in contaminatedthe main concepts environments of the applicatio by degradingn of endophytes hazardous in compounds.agriculture and We describebiotech- nology.the main concepts of the application of endophytes in agriculture and biotechnology. FigureFigure 1. 1. ProspectiveProspective biotechnological biotechnological applications applications of of endophytic endophytic bacteria. bacteria. 2. Types of Bacterial Endophytes 2. Types of Bacterial Endophytes Taxonomically, endophytic bacteria belong to 16 phyla comprising more than 200 Taxonomically, endophytic bacteria belong to 16 phyla comprising more than 200 genera. genera. However, the majority of them belong to the three phyla: Firmicutes, Actinobac- However, the majority of them belong to the three phyla: Firmicutes, Actinobacteria, and teria, and Proteobacteria [6]. They are either Gram-negative or Gram-positive, such as Proteobacteria [6]. They are either Gram-negative or Gram-positive, such as Pseudomonas, Pseudomonas, Achromobacter, Agrobacterium, Xanthomonas, Acinetobacter, Microbacterium, Achromobacter, Agrobacterium, Xanthomonas, Acinetobacter, Microbacterium, Bacillus, and BacillusBrevibacterium, and Brevibacterium[7]. Among others,[7]. Among mycoplasma others, mycoplasma has been isolated has been from isolated the cytoplasm from the of cytoplasmmarine green of marine algae (e.g., greenBryopsis algae (e.g., hypnoides Bryopsisor Bryopsis hypnoides pennata or Bryopsis)[8]. pennata) [8]. EndophyticEndophytic colonization colonization can can be be local local or or systemic systemic [9,10]. [9,10 ].The The plant plant endosphere endosphere repre- rep- sentsresents a protective a protective niche niche in inwhich which the the endoph endophytesytes are are protected protected from from biotic biotic and and abiotic stress.stress. Moreover, Moreover, endophytes endophytes can can ecologically ecologically adapt adapt to to their their environment environment and and overcome overcome plantplant defense defense responses responses [11]. [11]. BacterialBacterial endophytes endophytes can can also also be be classifi classifieded as as obligate obligate or or facultative facultative endophytes. endophytes. WhenWhen endophytic endophytic bacteria bacteria rely rely on on plant plant me metabolitestabolites for for survival survival and and transfer between between Plants 2021, 10, 935 3 of 33 plants vertically or through the activity of different vectors, they are defined as obligate endophytes [12]. In comparison, facultative endophytes live outside the host at a definite stage of their life and are usually transmitted to plants from the surrounding atmosphere and soil [13]. The data presented in Table1 show some examples of culturable bacterial endophytes and their attributes as plant growth-promoters. Table 1. Some examples of recently reported culturable bacterial endophytes and their attributes as plant growth-promoters. Host Plant/ Endophytic Bacterial Species Plant Growth Promotion Attributes References Organ Siderophores, IAA, ACC deaminase production, nitrogen fixation, Proteobacteria: Pseudomonas spp. Nicotiana tabacum/seeds [14] phosphorus/potassium solubilization, and trace metal tolerance Firmicutes: Rice (Oryza sativa Nitrogen fixation [15] Bacillus paralicheniformis L.)/roots IAA, ACC deaminase, amylase, Ammodendron Firmicutes: Bacillus mojavensis, Bacillus cellulase, protease, lipase production, bifolium/roots and [16] sp. phosphate solubilization, leaves nitrogen fixation Proteobacteria: Aquabacterium, Duganella, Massilia, Bordetella, Salmonella, Pantoea, Kosakonia, Klebsiella, Serratia, Pseudomonas, Agrobacterium, Stenotrophomonas, Sorghum bicolor/roots IAA production, fungicidal and Brevundimonas, Ancylobacter, [17] and stems bactericidal activities, nitrogen fixation Pleomorphomonas. Actinobacterium: Curtobacterium, Microbacterium, Nocardia, Sediminihabitans. Firmicutes: Bacillus, Micrococcus, Staphylococcus, Exiguobacterium Proteobacteria: Acetobacter, Burkholderia, Pinus arizonica; Pinus Production of active secondary Caulobacter, Pseudomonas, Ralstonia, durangensis/roots, metabolites, metabolism of vitamins [18] Bradyrhizobium, Methylocapsa phloem, and bark and cofactors Biosynthesis of active compounds with
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