Review: Endophytic Microbes and Their Potential Applications in Crop Management

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Article in Pest Management Science · September 2019 DOI: 10.1002/ps.5527

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James F White Kathryn Kingsley Rutgers, The State University of New Jersey Rutgers, The State University of New Jersey

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Rajan Verma Sofia Dvinskikh Rutgers, The State University of New Jersey Rutgers, The State University of New Jersey

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The user has requested enhancement of the downloaded file. a b Several experiments These effects of endo- 14,15 1,2,13 ., roots do not grow downward), and Rajan Verma, i.e a The re-inoculation of axenic or near axenic Satish K Verma, Root hair elongation may be triggered by It is unknown what is produced or degraded a 14,15 21 21 medium, provided the original work is properly cited. Correspondence to: JF White, Department of59DudleyRoad,NewBrunswick,NJ08901,USA.E-mail:[email protected] Plant Biology, Rutgers University, Department of Plant Biology, Rutgers University, New Brunswick, NJ, USA Centre of Advanced Study in Botany, Banaras Hindu University, Varanasi, India U.S. Geological Survey, Great Lakes Science Center, Cleveland, OH, USA ∗ c a b Qiuwei Zhang, seedlings frequently are diminishedroot hair in formation. size with reduced or no be another reflection of co-evolutionaryand association plants. of microbes Controlledgrasses experiments cleaned revealed of that mostroot gravitropic seedlings of response ( their of endophytic microbes lose the seedlings with microbes that internallyin colonize seedlings reacquisition results ofplant gravitropic stature response and root of hair development. roots and increased suggest that rootejected hairs from elongate hairs. until all microbes have been by the intracellular microbesin to seedling initiate roots. the Endophytic gravitropic microbesshown response to in enhance plants root have growth alsother and leading been increase to increased root plant branching, growth. fur- nitric oxide or ethyleneprotoplasts that production cluster in by the tip the of the elongating intracellularnot hair, but been microbe this has proven. phytes on rootof growth growth are regulators generally by attributed microbes; to however, enhanced production nutrient c a 16 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. All 9–11 1,2 Endo- 4 Matthew T Elmore, a The particular published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. 16 Other endophytes (iv) modulate plant 3,4 12,13 Pest Management Science and Kurt P Kowalski Kathryn L Kingsley, b a* Sofia Dvinskikh, Pest Management Science a © 2019 The Authors. and (v) suppress weed growth. 13–15 (ii) defend plants from pathogens and insects, biostimulants; bacteria; endophytic microbes; fungi; microbiome; rhizophagy cycle 5–8

2 EFFECTSGROWTH OF MICROBES ON PLANT 2.1 Endophytes modulateModulation plant development of seedling development byresult endophytes is of likely the the microbes evolution that of plants colonizepate in plant in continuous tissues the symbiosis andmany development with microbes thus process. to produce reliably The plantoxide) partici- widespread signal molecules growth capacity (such regulators of as nitric (such as auxins and ethylene) could In this review, we discuss the functionsnisms of of endophytes, the activities mecha- of endophytes, andtions current of endophytic and microbes future in applica- crops. (iii) increase stress tolerance in plants, 1.1 Overview ofAn endophytism in endophyte plants is anyinhabits microbe internal (typically tissues fungal of or plants bacterial) without that causing disease. 1 INTRODUCTION Keywords: Endophytes are microbesfunctional (mostly in bacteria that and theyof may fungi) plants, suppress carry present virulence in nutrients pathogens, asymptomatically increase fromspecies. disease in the Endophytic resistance microbes in soil have plants. plants, been and into suppress shown Endophytic development to: plants,cycle of (i) and microbes modulate competitor obtain other plant nutrient-transfer nutrients plant are symbioses; in (ii) development, soils increase often and plant increaseprotect growth transfer plants and stress nutrients from development; to disease; (iii) tolerance (v) reduce plants oxidative deter in stress feeding the of byeffective hosts; rhizophagy herbivores; functions (iv) and of (vi) endophytic suppress microbes, growth we of suggest competitor plant that(fertilizers, species. endophytic fungicides, Because microbes insecticides, of may the significantly and reduce herbicides) use in ofplants the agrochemicals cultivation during of domestication crop plants. and Thecrops loss long-term to of crop cultivation endophytic species. microbes could from Increasing crop repression be atmospheric of carbon remedied reactive dioxide oxygen by levels used could to transfer© reduce extract of 2019 the nutrients The from efficiency endophytes Authors. microbes of from in the roots. wild rhizophagy cycle relatives due of to Surendra K Gond Abstract potential applications in crop management James F White, Nkolika Obi, Review: Endophytic microbes and their (wileyonlinelibrary.com) DOI 10.1002/ps.5527 Mini-review Received: 15 March 2019 Revised: 19 June 2019 Accepted article published: 22 June 2019 Published online in Wiley Online Library: 27 July 2019 may be recruited from the soil but similarly benefit plants. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any mechanisms by which endophytic microbestions fill in plants the likely various differ func- depending on the microbe and plant. or most plantsphytes possess are endophytes, seed transmitted andplant and in health begin most to as promote cases soon growth endo- as and seeds germinate. phytic microbes are importantfunction components in of the plants,by and following plants, they ways: (i) increase nutrients acquired development,

2558 2559 via and In the 21 e. (B) Shows This proto- 23 Microbes acquire Microbes are inter- 21 The mechanism by 21 21 ) around the periphery of 1 m;stainedwithDABfollowedby − μ s 20 μ = wileyonlinelibrary.com/journal/ps Microbe protoplasts are circulated rapidly Any nitrogen fixation by microbes involved 23 ., carbohydrates, proteins, vitamins, organic 21 e.g m; stained with fluorescent nucleic stain SYTO 9). Figure from Exposure to reactive oxygen (superoxide) produced μ Suppression of superoxide formation in plant roots using 20 21,22 = 18 free-living walled phase in the soil (Fig. 1)-(C). elevated carbon dioxide results in failureto convert of to microbes protoplast in phases root (J. White, cells lished). R. Verma, Protoplast N. forms Obi, Unpub- ofin microbes root ‘bud’ cells or as they ‘bleb’ replicateoften sequentially with being older microbe oxidized cells/protoplasts completely –cells swelling age and (Fig. disappearing 2(B)). as by root cellsmicrobes; triggers bacteria the form protoplast loss phasesfungi of called form ‘L-forms’, cell protoplast while phases walls termed by ‘mycosomes’. the intracellular in the rhizophagy cycle likelybecause occurs high in levels the of free-livingplasma soil membranes reactive phase onto oxygen microbes secreted inhibit from nitrogenases. root cell nutrients in thetively free-living soil extracted phase fromprotoplast and microbes phase. nutrients in are the oxida- endophytic/intracellular plast phase may be comparedare also to microbe the phases bacteroids involved ofcells. in rhizobia nutrient that exchange with host rhizophagy cycle, microbes areroot provided nutrients exudates by ( plants acids) around the root tip meristem (Fig. 2)). which microbes areHowever, once internalized internalized intoperiplasmic microbes space, root become between cells cell situatedroot wall is cells, in where and unknown. root plasma the cellscell membrane secrete of plasma superoxide produced membrane byAdenine root bound Dinucleotide Phosphate NADPH2(B)). Oxidase) oxidase onto (Nicotinamide microbes (Fig. (circulation estimated at 8–11 nalized into meristematic root cells thatcell do walls not have just fully beneath formed the exudate zone. In this Because 20 17,18 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. : 2558–2565 © 2019 The Authors. Pest Management Science 75 Another type of nutritional endophytic symbio- 6 (3): 95. https://doi.org/10.3390/microorganisms6030095. (2018). 2019; Another nutrient acquisition mechanism involves 18 19 Diagrammatic representation of the rhizophagy cycle. (A) Diagram of the rhizophagy cycle showing microbes entering root cells at the root tip 20 aniline blue). (C) Bacteria (arrow) emerging from root hair tip of grass seedling (bar Microorganisms the liberation of nutrientsbetween, from or insects cycle by between, microbes plants that and decaying extend insects. Pest Manag Sci a free-living soils phase; soil nutrientsbacteria are (arrow) acquired in in the the periplasmic free-living space soil of phase parenchyma cell and near extracted root oxidatively tip in meristem the of intracellular an endophytic Agave phas sp. seedling (bar Figure 1. meristem and exiting root cells at the tips of elongating root hairs. Rhizophagy cycle microbes alternate between an intracellular endophytic phase 3.2 Rhizophagy cycleIn and nutrient another acquisition symbiosis, the ‘rhizophagybiosis’, cycle’ microbes or ‘rhizophagy (often sym- endophytic/intracellular bacteria protoplast or phase yeasts) in cycle root between cells an and a 3.1 Nutrient transferEndophytic symbioses microbes that bring nutrientsthat to fix plants atmospheric nitrogen include in those plant tissues. Thesephytes types include of endo- actinorhizal and rhizobial symbioses. 3 NUTRITIONALENDOPHYTES FUNCTIONS OF Endophytic microbes and their applicationsacquisition from microbes mayplant equally growth. contribute to enhanced www.soci.org process insects consume plants, accumulating nitrogen andnutrients other in their bodies; degradationare of insects also by symbiotic microbes that withplants. plants results in transfer of nutrients to sis involves microbes thatextend inhabit out both into endophytic soil.fungi establish tissues Dark this and kind septate of symbiosis endophytesHyphae with and many families of mycorrhizal of plants. thesemycelia fungi extending into grow soil acquire endophytically nutrientsto and in mobilize plants. it roots, back and the of sensitivity of nitrogenases to oxygen,that the engage few families in of nitrogen-fixing plants low symbioses oxygen sequester nodules microbes – where in root nitrogen is tissues. fixed and transferred to 28 via et al. Trifolium sp. showing : 2558–2565 75 ., iron, copper, Many microbes e.g The entry of the 28 );stainedwithaniline 2019; 28 Pseudomonas spp., have the capacity to Unlike nodule-forming sym- ). (D) Root hairs of clover ( 27 μ Pest Manag Sci 15 Bacillus = Phragmites australis Metals also adhere to the cell walls of 27 27 inoculated with bacterium These organic acids have a high affinity for metals, 28 spp.) possess high affinity transporters that enable Bacillus ., Cynodon dactylon e.g ). microbes; here rhizophagy cycle suppressionabsorption resulted in into reduced seedlingsWhite, of R. potassium, Verma, calcium N.acquisition Obi, of and difficult unpublished). sulfur to However, obtain (J. itzinc) micronutrients ( is may a be key that functionsiderophores of and the other rhizophagy mechanisms cycle.ents Microbes that efficiently possess sequester and micronutri- manyacquiring are nutrients. motile and move around in soils them to detect and absorb these organic acid-metal complexes. 3.3 Plants usePlant microbes roots to mine secrete for organic soil acids, metals includingand malic acetic acid. acid, citric acid, Microbes benefit nutritionally by absorbing the organic acid-metal complexes, in that theyacids, acquire and carbon mineral nutrients in nutrients the simultaneously. organic microbes because microbe cell wallswhile have metals have a a net positive charge. negative charge, including iron, zinc, copper, and magnesium. microbes into the root cellsfrom the permits microbes. Harvesting plants of metals to from extractthe the soil the rhizophagy microbes metals cycle likelyneeded gives for plants sustenance and the growth critical (Fig. 3)). soil nutrients 3.4 Rhizophagymicrobes microbes take nutrients from other soil Rhizophagy microbes, such as extract nutrients from other soil microbes by causing nutrient ( bioses, the rhizophagy cycleplants and appears likely to represents an occur importantacquisition in mechanism by plants. for most nutrient vascular μ 15 = www.soci.org JF White © 2019 The Authors. s showing replicating protoplasts of bacteria (arrows) in the periplasmic space of the cell The constant 21 ). (C) Root hair of grass sp.) showing yeast being expelled from the root hair tips (black arrows) and yeast protoplasts within μ Gene responses of P. australi 15 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. = Cyclosis of protoplasts 24–26 21 Rhodotorula The stimulus that triggers root hairs to 21 Pest Management Science These upregulated genes may be the result of 7,8,13 Microbes in plant roots. (A) Cloud of bacteria (arrows) around root tip meristem of invasive reed grass ( ) inoculated with endophytic yeast ( In the rhizophagy cycle, plants cultivate microbes that func- wileyonlinelibrary.com/journal/ps blue (0.1% aqueous). (B)(stained Root with parenchyma DAB, cell followed of bybacterial protoplasts aniline (arrows) in blue; the bar periplasmic space of the hair (stained with DAB, followed by aniline blue; bar root cells through the action of cyclosis. Figure 2. repens root hairs (white arrow) (stained with DAB, followed by aniline blue; bar increased oxidative reactions in rootsnitrates and resulting increased from liberation protein of degradation.involving Another tomato seedlings experiment employed elevated carbonsuppress dioxide superoxide to formation and extraction of nutrients from results in increased replication ofsmall microbe protoplasts protoplasts with being many formedmicrobe from cells. fewer original Exposure intracellular ofreactive oxygen intracellular results bacterial in electrolytetoplasts, protoplasts leakage and to from bacterial oxidized pro- bacterialthrough the components plasma membrane may by plant be root cells. absorbed periodically eject microbe protoplasts islikely unknown. mechanism of However, the ejection maythe involve potassium vacuole loading at into basein of the the hair vacuole hair that cellforcibly propagates expelling with from microbe protoplasts the consequent from hair expansion the base hair. to the tip, tion as carriersexperiment of nutrients it and wasmately support 30% found plant of that nitrogen growth. from grass In rhizophagy. plants one obtained approxi- circulation of microbes againstmay reduce the nutrient gradients root between microbe cell and roottoplasts, plasma cell resulting pro- membrane in more efficient nutrienttwo transfer cells. between Surviving the intracellular microbesroot that hair accumulate tip in trigger the the elongationoxide of signaling) root and hairs microbe (perhaps protoplasts byejected are nitric periodically through forcibly pores that formreforming in their root hair cell tips walls –rhizosphere as with (Fig. microbes they 2(C,D)). reenter soil populations in the plants infected with endophytesidants often and show nitrate thatin transporters plant plants. are antiox- among genes upregulated

2560 2561 2 ts of on 2 in air to cavenging 2 Carbon dioxide 21 by 50% in air around 2 levels as is exhibited in in the atmosphere may 2 2 wileyonlinelibrary.com/journal/ps scrubbers to locally reduce CO 2 is sequestered into 4-carbon oxaloacetate 2 Increasing the level of CO 33 on the rhizophagy cycle. Potential future solutions to coun- 2 nutrients from microbes that enter root cells. and moved into bundle sheathreactive cells thus oxygen is formation. unavailable to If inhibit the suppressive effect of CO plants with C-4 photosynthesis. 5 APPLICATIONS OFAGRICULTURE ENDOPHYTES IN 5.1 Plant domesticationPlants and loss in of endophytic microbes naturalwith communities maintain endophytic symbiotic microbes associations that support growth and protect sensitivity. It is also possible that plantssensitive may evolve to to become increasing less atmospheric CO seedlings of wheat, tomato,photosynthesis and pathway) tall substantially fescuereactive seedlings reduced oxygen (superoxide) (with secreted the by C-3 root amount cells ontoresulting microbes, of in fewermicrobes nutrients (J. White, being R. Verma, extractedsynthesis N. plants, from Obi, unpublished). CO intracellular In C-4 photo- nutrient extraction from microbesiments, is then supported in increasing future levels exper- of CO teract decreased efficiency ofmicrobes oxidative could nutrient be: (1) extraction the use from ofantioxidants and soil are microbes more that susceptible produce to oxidative fewer nutrienttion; extrac- (2) the use of CO levels that are optimal forment of the techniques/technologies to rhizophagy increase oxygen cycle; levels around (3)plants the or develop- plant roots to increase efficiencyeration of in reactive the oxygen gen- rhizophagy cycle;that or show increased (4) root reactive the oxygen secretion development or reduced of CO plants cause agricultural scientists to seekof CO ways to neutralize the effect suppresses formation of superoxidefrom needed microbes. to extract nutrients levels on 2 This effect of 32 published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. on NADPH oxidase involved in 2 levels and reduced efficiency 31 2 spp. and some other bacteria colonize This capacity of some microbes to tap into levels, having reduced content in nitrogen : 2558–2565 © 2019 The Authors. 2 spp. frequently possess hemolysins that are Pest Management Science 4,13 level and the efficiency of nutrient extraction 75 Bacillus 2 2019; C-3 photosynthesis pathway plants are particularly Bacillus 32 29 (A,B) Beneficial outcomes and nutrient flow in the rhizophagy symbiosis. (A) Beneficial outcomes include: (i) Plants obtain nutrients from In the soil 30 in reducing nutrient acquisition by plants may be explained 2 lipopeptides, which act as biosurfactants thatporosity increase membrane and induce nutrient leakage fromfungi. affected cells, typically the rhizophagy cycle. Asmarily described superoxide) above, in reactive the oxygen rhizophagy (pri- cycle functions to extract Pest Manag Sci flowing from plant roots to soil microbial community; rhizophagy microbes carry nutrients from the soil microbial community back to the plant. 4 CARBONRHIZOPHAGY DIOXIDE CYCLE SUPPRESSION OF 4.1 Rising atmospheric CO of nutrients from soil funginutrient by flow, rhizophagy rhizophagy microbes mediate microbes between results the plant in and reduced the soil virulence microbial of community, with potential photosynthate and pathogens other in plant-abundant nutrien the soil microbial community. (B) In terms leakage from their cells.contained in This the enables soil microbial thements community to and back carry access those to nutrients nutri- nutrients from the other microbes plant using ‘hemolysins’that (biosurfactants) (Fig. form 3(B)). pores Rhizophagynutrients. in microbes microbe membranes, take causing them to leak Figure 3. internalized microbes; (ii) Increased production of reactive oxygen in roots results in increased oxidative stress tolerance in plants; and (iii) S Endophytic microbes and their applications www.soci.org by the suppressive effect of CO of the rhizophagy cycle Recent research on the effects of rising atmospheric CO and minerals including magnesium, zinc, and iron. nutrients contained in soil microbes emphasizes the importance of a diverse and healthy soil microbialintegrate community. into In the a sense, soil plants microbialfixed community nitrogen as flow soil from soil nutrientssynthate microbes and from to plant plants roots and flows thennity out photo- (Fig. to 3B). the Microbes soil involved microbial inalso commu- the solubilize or rhizophagy make symbiosis available other may nutrientsthat in the are rhizosphere absorbed by the plant. from soils. affected by high CO nutrient content of majorship food between crops CO shows an inverse relation- CO hyphae of soil fungi and use lipopeptideshyphal to membranes. induce leakage in the 52 At ;in The The Fes- et al. 44 Endo- 47 48 infected 49 . SOD C : 2558–2565 75 Species of fun- and Endophytic fun- 52 44 Some endophytes The release of ROS 2019; 44 SOD B 44 , The upregulation of host The infection of soybean 44 s significantly reduced lipid sp. 638 isolated from stems 50 were upregulated in leaves of Piriformospora indica SOD A (Clavicipitaceae) intercellularly A q-PCR analysis showed that ., leaves, culms, and seeds) and A meta-genome analysis of rice 45 Pest Manag Sci Pestalotiopsis microspora ) treated with polyethylene glycol 44 i.e 46 has been shown to induce abiotic ANAC072 Epichloë Enterobacter and have higher concentrations of osmoprotec- The expression of drought-protective genes Brassica rapa 46 ) grass tissues infected by the endophytic fungus Paecilomyces formosu RD29A 43 , Endophytic symbionts also may improve plant resis- 51 CBL1 , 41–43 Piriformospora indica a ‘quorum-quenching effect where pathogenic fungiulent remain rather avir- than causingpounds disease. produced Many of byinducing the endophytes nutrient antifungal target leakage, com- membranes resultingfungi. in of reduced fungi, virulence of the endophytes showed the presence ofenzymes numerous involved genes in encoding glutathione protection synthases from and excessive also glutathione-S-transferases. ROS, including 5.4 Endophyte-mediated anti-herbivory Some endophytes produce andreduce fill herbivory by plants insects and with other herbivores. compounds that These endophytes have found application in increasingance pest in toler- commercial forage and turf grasses. However, endophytes 5.3 Endophytes alterEnvironmental oxidative stress stresses tolerance in trigger plants plantgen cells species to (ROS; formhydrogen including reactive peroxide, superoxide, oxy- and hydroxyl hydroperoxyl radicals). radicals, bacteria at the earlytranscript stages levels of of colonizationdismutase ROS-degrading caused and upregulated genes glutathione reductase. including superoxide gus stress tolerance in many plants. Chinese cabbage ( to mimic drought stress,enzymes exhibited peroxidases, upregulation catalases, ofleaves and within antioxidant 24 superoxide h. dismutases in tuca arundinacea Epichloë coenophiala tive mannitol and other antioxidant fungal carbohydrates involved in protection of plants under oxidative stress. ROS-degrading genes may furtherplants by reduce pathogens oxidative that induce damage or produce to ROS. Tall fescue ( peroxidation, and increased formation ofoxidase, peroxidase, polyphenol catalase, and superoxide dismutasesubstrates. in Ni contaminated by endophytic tance and protect plants against aparticularly broad through induced spectrum systemic of defense pathogens, (ISR)ing by upregulat- salicylic acid (SA) andor jasmonate PR proteins. (JA) pathways and ethylene DREB2A endophyte-containing plants. phytes are also reported toplants reduce in oxidative metal stress generated contaminated in soils. gal endophytes in genus inhabit aerial parts ofproduce plants a variety ( of alkaloids that deter feeding by herbivores. induce stress tolerance to both biotic and abiotic stresses. endophytic bacterium of poplar trees wassuperoxide dismutases, shown including to haveaddition it genes possessed that genes encodetases, for several catalases, hydroperoxide hydroperoxide reductases, reduc- potent and antioxidant thiol compoundsbeen peroxidases. pestacin isolated from and endophytic isopestacin have early stages of endophytic colonization,are plant defense activated, responses producing ROS. within plant tissues and cells canproteins, cause oxidative damage nucleic to plant acids, and membranes. are www.soci.org JF White © 2019 The Authors. Cynodon Bacillus This involves Pseudomonas, 21 This may result in There are increas- 15 41 However, symbiotic produce a variety of published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. 38,39 34–36 Modern hybrid maize varieties Species of genus The high levels of diseases and 36 38 41–43 P. fluorescens, Reacquisition of those microbes from and 37 . A variety of lipopeptides that they pro- We do not know the effects of long-term , it was found that 7 years of continuous 11 41 Pest Management Science Bacterial endophytes of genus Alternaria 39–41 Some grass seeds, such as Bermuda grass ( Acquisition of microbes from seeds of uncultivated P. aeruginosa and 36 ) are routinely cleaned of the microbial rich seed husk 38 upregulation of host defense genes. Nicotiana attenuata) antifungal compounds, including2, 4-diacetylphloroglucinol, phenazine-1-carboxylic pyrrolnitrin, acid, pyoleutirin andlike volatiles hydrogen cyanide compoundsgrowth that of significantly fungal inhibit pathogens. the important disease control agents becauseety they of synthesize a biologically vari- activeof molecules phytopathogens. that are potential inhibitors wileyonlinelibrary.com/journal/ps 5.2 Mechanismssuppression for endophyte-mediated disease Among the many ways that endophytes improve plantis health, one by suppressing pathogen growth and fitness. plants against biotic and abiotic stresses. including wild populations of thecultivation tobacco resulted and in application to resistanceof seedlings to cotton in the seeds to disease. removemicrobes, Acid fibers leaving treatment removed cotton natural seedlings more seed-vectored vulnerabledisease. to stress and plants in the cottonresistance family in greatly cotton improved seedlings. stress and disease duce induce leakage inreduces their virulence fungal as pathogens hyphal of plants. membranes that greatly use of inorganicon fertilizers, endophytic fungicides, microbes orlong-term in agrochemical other use crop has agrochemicals plants caused aphytic and loss microbes of it symbiotic from endo- is manycomponents crop possible of species. that the The losshow natural of the endophytic individual seed communityseeds community could that alter of are microbes lesslosses functions of capable and essential of result endophytic growthagrochemicals microbes in in and crop and survival. cultivation, reduce it To reliance couldendophytic microbes be remedy on from necessary wild to relatives obtain ofthem crops into and crops reintroduce – perhaps as seed treatments. microbes may be losttivation. during In domestication a cropping and experiment( long-term using cul- an annual wild tobacco cultivation and seed cleaning, resultedand in increasing levels symbiotic of microbe disease due loss to fungalFusarium pathogens in genera require higher inputs of nitrogen andthan pesticides older to flint-type produce Indian crops maize orbe tropical maize the – result and this of may lossvarieties. of symbiotic endophytes from hybrid maize several mechanisms includingtion direct with pathogens antagonism for space byof and antimicrobial nutrients competi- through metabolites production andresistance through or induction increasing of systemic resistancevia in plants against pathogens ing numbers of studies thatbacteria) suggest provide that defense endophytes to (fungiother host and pests plants against beginning pathogens atof and seed the germination plant. and lasting the life and covered with fungicides, leaving grass seedlingsnatural without their endophytes. dactylon pests that plague cotton couldotic be microbes the from result cotton of seeds. theintensively Crops loss such of cultivated as symbi- and maize have modifiedseed been to structures the that extent vectorancestral teosinte that microbes have been like external lost. hulls once present in

2562 2563 Phragmites To facilitate Recently, the a competitive 59 57 P. australis 1,7,8,35,45,46,58 The symbiotic relationships 57 wileyonlinelibrary.com/journal/ps but the location and roles of individual 57 The scientific, legal and regulatory frame- 59 ., through the rhizophagy cycle), while simultaneously (common reed), a strategy that could be adapted for other e.g agenda was developed to evaluate how thecould microbial be community targeted as aaustralis form of control forinvasive non-native and weedy plant species. microbes within the plant are still unclear. 6 CONCLUSIONS Microbial endophytes andto soil improve plant microbescommercial health could crop and be plants. enhanceendophytes Benefits employed reduce productivity could pathogens, insect directly also damage,with in weedy be and plants. competition realized Increasing crop when productivitythe without health harming of agriculturalwith agrochemicals soils can be and a compromisingpractices. challenge The using food current present efforts agricultural quality to finda microbial beginning crop that stimulants are may leadapplications to in a crop production. significant Endophytes reductioncrops could in help with chemical cultivate less fertilizers,In fungicides, the insecticides, future, we or envisionthe herbicides. a optimization of change the in relationship practice ofendophytes. plants to Supplementing to focus microbial soil more diversity microbes and on through microbe amendments to soils and plants that functionplants to bring ( nutrients to suppressing virulence inand pathogens, reducing deterring growthenvironmental insect of contamination and feeding, competitor agricultural weeds,more practices that can parsimonious are with result naturalfuture, in we processes. must less To develop a bring betterfunction understanding about of in this how microbes soilsoptimize and microbial in functions plants.protection. to We enhance must crop further production learn and how to 5.7 Hindrancesin and agriculture advances in applications of endophytes The lack of an overallmunities awareness of of the endophytic general microbes presence inhindrance of in tissues com- advancing exploration of of plants applications of hasin endophytes crops. been Add a to this,most microbes the on general plants are and pathogenic prevalent orhas have assumption contributed negligible to effects that lack of effortsphytes to in understand plant the growth roles promotion of and endo- plantOver health improvement. the past fewof decades research the that gradual demonstrated developmentplants that of and endophytes a positively are body affect commonresents in plant an important development advancement and intance health understanding and rep- the functionality impor- of endophytes. development of applications for microbes in agriculture, the recent U.S. government 2018 Agriculture Improvementas Act the (also known 2018 Farm Bill)ments in in the the United European Statesand Union and their explicitly regulation. regulatory addressed docu- biostimulants work appears to be inments place for in some products significant and futureagriculture. advance- applications of endophytic microbes in exploration for useful endophytes and othertural microbes for applications agricul- has beennies enhanced that by have emergence as ofing their compa- of primary plant focus biostimulants development (including and endophytes). market- with its endophytes give the non-native edge over native species, It Fur- 53 Pseu- 56 spp. Burkholde- Similarly, in Recently, an 52 57 Fallopia japon- , (Amaranthaceae), , reducing native Fusarium , originally isolated ), isolated from roots , which colonizes the published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry. Amaranthus hypochon- Poa annua , (Pleosporaceae) produce the Further, an endophytic ) in the morning glory family gene encoding endotoxin for 53 cynodontis Froelichia gracilis In a case of endobiome interference, Micrococcus luteus 56 Undifilum subsp. Taraxacum officionale) Periglandula : 2558–2565 © 2019 The Authors. Aureobasidium pullulans ‘Endobiome interference’ occurs where entry and Pest Management Science In another example, an endophytic 75 Phragmites australis 56 54 WCS358r was modified with an antifungal gene instar silkworms. JK-SH007 was transformed with the Bt endotoxin 2019; These few examples suggest that endophytes that Bacillus thuringiensis Clavibacter xyli 52 When introduced into plants other than their adapted Genes introduced into endophytic microbes could confer , resulting in growth repression of the seedlings. 55 53 Rumex crispus, Bombyx mori , host, some endophytic microbes can cause growthdeath repression and in seedlings. a fungal endophyte ( of a weedy yet native species was introduced by seedling inoculationof into seedling roots the of the cells exotic plant and species tissues driacus new characteristics, which maypathogens, be growth useful promotion in of bio-control hostof of plants, medicines for plant and/or humans production or animals.bacterium For example, the endophytic xylem of severalexpress plant the species, wascontrol transgenically of insects. modified to Pest Manag Sci Endophytic microbes and their applicationsof this group of organisms aregal limited endophytes to grasses (genus and sedges. Fun- www.soci.org (Convolvulaceae) have been also shown to produce ergot alkaloids that make morning glories highly toxic to herbivores. of non-adapted microbial endophytes into plantresults in cells repressed plant and growth and tissues disruption of functionsendophyte-host of symbiosis. the plants commonly referred to as ‘locoweeds’ in the familyendophytic Fabaceae, fungi in genus toxic alkaloid swainsonine, a powerfuland anti-herbivore toxin. compound ria pyrrocinia gene to express the insecticidalof protein against the second stage 5.5 Transgenic endophytes Transgenically modifying endophyte genomes couldstrategy be and a an useful alternativeplant. to genetic manipulation of the host deter feeding by insect pests may be morecurrently common than documented. has been A moreand thorough bacterial examination endophytes in of plants fungal tional may endophytes result that may in be numerous used addi- infeeding crops or to improve reduce plant insect tolerance pest to feeding. and introduced intogal wheat populations with in a soil, including resultant pathogenic reduction in fun- domonas putida 5.6 Endobiomegrowth interference as a strategy to reduce weed The symbiotic relationships betweenphytic a microbes host are plant unique, which andplant. can its become endo- a liability for the seems likely that futurethe exploitation efforts of transgenically to modified endophytes. managedue However, to crops the could mobility involve microbes of to endophytic specific plants microbes may containment be difficult of or the impossible. ther, the bacterial endophyte ica endophytic bacteria and reducinginterference seedling could growth. be Endobiome acommunities common and could phenomenon be in onecompetitor way natural that plants. plant plants Similarly, reduce if growth used of endobiome as interference a management may treatment, havesive potential character to of reduce invasive and the weedy inva- plant species. from tomato seeds andwhere seedlings, they was entered transferredspecies into to (including seedlings seedling root cells of multiple plant , , , et al. et al. et al. ,Col- et al. 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SKV to and authors SKG were to funded improve by UGC,Raman the India Post in Doctoral the form fellowships of to conductauthors research also in received USA. support The fromW4147, USDA-NIFA and Multistate the Project New Jersey Agricultural Experiment Station.for Funds much of this workUnit were from CESU Cooperative G16 AC00433 Ecosystems between Studies RutgersGeological University Survey and for control the of U.S. invasive ACKNOWLEDGEMENTS use of trade, firm, or product names is forand descriptive purposes does only not imply endorsement by the U.S. Government.

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