Plant rootmicrobe communication in shaping root m

Authors: Andrew Lareen Frances Burton Patrick Schäfer

Publish Date: 2016/01/04

Volume: 90, Issue: 6, Pages: 575-587

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Abstract

A growing body of research is highlighting the impacts rootassociated microbial communities can have on plant health and development These impacts can include changes in yield quantity and quality timing of key developmental stages and tolerance of biotic and abiotic stresses With such a range of effects it is clear that understanding the factors that contribute to a plantbeneficial root microbiome may prove advantageous Increasing demands for food by a growing human population increases the importance and urgency of understanding how microbiomes may be exploited to increase crop yields and reduce losses caused by disease In addition climate change effects may require novel approaches to overcoming abiotic stresses such as drought and salinity as well as new emerging diseases This review discusses current knowledge on the formation and maintenance of rootassociated microbial communities and plant–microbe interactions with a particular emphasis on the effect of microbe–microbe interactions on the shape of microbial communities at the root surface Further we discuss the potential for root microbiome modification to benefit agriculture and food productionAll eukaryotic organisms are influenced by complex interactions with microbial communities The potential for gut microbiota to affect the health and nutritional status of host animals is well documented Cummings and Macfarlane 1997 Hooper et al 2002 Flint et al 2012 and it is known that these microbial communities can be deliberately manipulated or inadvertently influenced through factors such as host diet Turnbaugh et al 2009 antibiotic use Willing et al 2011 and fecal transplants Song et al 2013 Like the animal gut the primary organ for nutrient and water uptake in plants the root system is populated and surrounded by a complex microbial community referred to as the root microbiome Hacquard et al 2015 Interactions with the root microbiome have the potential to influence plant health and development Berendson et al 2012 PankeBuisse et al 2015 Direct interactions may range from parasitic as is the case with soilderived plant pathogens through to mutualistic symbioses Indirect effects are also of considerable importance Microbes are key players in nutrient cycles and aid in nutrient acquisition Mishra et al 2012 Bulgarelli et al 2013The importance of interactions between particular plants and specific microbial species is not a new concept Beneficial symbiotic relationships such as between legumes and nitrogenfixing microbial symbionts have been recognized for some time Bergersen 1971 as too have the detrimental effects of plant pathogens on crops Oerke 2006 Aside from the effects of specific pathogens and symbionts on plant health recent research has indicated that the composition of microbial communities at roots the so called root microbiome can have significant impacts both on plant development and their stress tolerance Mendes et al 2011 PankeBuisse et al 2015 Some consider the root microbiome a “secondary genome” that provides host plants with microbederived compounds and traits Berendson et al 2012 Rout and Southworth 2013The root microbiome is recruited from a diverse range of microbes present in the surrounding bulk soil soil biome outside the rhizosphere The emergence of dominant groups in the rhizosphere from this soil biome can have major implications for resident plant species While soil biomes are undoubtedly a key determinant of root microbiome composition research has demonstrated that host genotype also influences the overall composition of these communities Badri et al 2013 Bulgarelli et al 2012 2015 As it is largely plantderived exudates and substrates that provide the nutrients and physical niches of the rhizosphere it perhaps makes evolutionary sense that plants should have adapted to influence this ecosystem to their benefit However opinion is divided as to whether it is edaphic factors or selection by plants that are the greatest determinant of root microbiome composition What is clear however is that both edaphic and hostplant factors exert strong influences over its formation Chaparro et al 2012 Hacquard et al 2015 Rootassociated microbial communities have been the focus of much research However the factors and multipartite interactions that can lead to changes in root microbiome structure and hence affect plant health and development are highly complex dynamic and not fully understood Exploiting the beneficial potential of the root microbiome can provide sustainable solutions in raising agricultural crop production Philippot et al 2013 In particular diseases caused by soilborne microbes have a major negative impact on global crop productivity and account for major losses in wheat rice potato maize and soybean Oerke 2006 Raajmakers et al 2008 Alexandratos and Bruinsma 2012 In the context of increased demand for food by an expanding human population coupled with reductions in cultivable land and agricultural productivity due to development and climate change effects Alexandratos and Bruinsma 2012 understanding the interaction of plants with microbial communities and development of methods for manipulation of microbiome composition to encourage plantbeneficial relationships is increasingly relevant This review provides an overview of what is known about microbial community dynamics with a detailed focus on the potential for manipulation of the root microbiome to increase crop yields and reduce losses to biotic and abiotic stresses In addition to introducing briefly the effect of plants and soil on microbome composition we will particularly discuss the effect of microbial interactions on microbiome composition and dynamicsSoil type and plant roots can determine the composition of microbial communities associated with roots though their quantitative contribution in influencing rhizosphere communities rhizobiome is unclear The effect of soil and plants on the composition of rhizosphere communities has been excellently reviewed recently Berg and Smalla 2009 Philippot et al 2013 Bulgarelli et al 2013 2015 and therefore only an overview is provided here Soils can vary in pH structure texture organic matter content microaggregate stability and the availability of nutrients These physicochemical properties of soils can directly select for specific microbes by creating niche environments that benefit certain types of microbes and influence the availability of plant root exudates affecting microbial recruitment by the plant For instance soil pH and nutrient availability eg carbon nitrogen phosphate have been found to affect the abundance of crop pathogenic bacteria fungi and nematodes as well as beneficial microbes Höper et al 1995 Duffy et al 1997 Lacey and Wilson 2001 Rasmussen et al 2002 Rimé et al 2003 Hamel et al 2005 Rotenberg et al 2005 Toljander et al 2008 Dumbrell et al 2010 In most extreme cases soil characteristic might result in soil typespecific composition of rhizosphere microbial communities Garbeva et al 2004 Consistent with this Gelsomino et al 1999 have shown that the structure of bacterial communities was similar in soils of the same type rather than geographical location and Latour et al 1996 observed that soil type affected the diversity of Pseudomonas spp associated with flax and tomato plants This indicates that soil type and soil characteristics can influence which microbes dominate the rhizosphere and that different types of soils can harbour diverse microbial communitiesSignificant effects on the composition of rhizosphere communities have been assigned to soil types and plant species Chiarini et al 1998a b Grayston et al 1998 Buyer et al 1999 Dalmastri et al 1999 Miethling et al 2000 Smalla et al 2001 da Silva et al 2003 Rasche et al 2006 Bulgarelli et al 2012 Lundberg et al 2012 Peiffer et al 2013 Tkacz et al 2015 suggesting a hierarchic contribution of soil and plant species on microbial communities Bulgarelli et al 2013 Philippot et al 2013 Schlaeppi et al 2014 Whereas physicochemical properties of soil types determine the composition of soil biomes plant root exudates can create an environment at the rhizosphere that gradually alters the soil biome to favor the establishment of a rhizobiome These exudates together with the root immune system would finally select for those microbes that due to further adaptation have evolved mechanisms to colonise the root rhizoplane and/or inner root tissue endosphere Endophytes or colonisers of the rhizoplane can have detrimental or beneficial effects on plant species and resulting changes in the structure of the plant community would feedback in the composition of the rhizobiome Bever et al 2012 In such a model in addition to soil properties plant exudates and microbial activities would determine the magnitude of biome conversion Bever et al 2012 Bakker et al 2013 Bulgarelli et al 2013 Philippot et al 2013 Further recent studies highlighted the significance of hormones involved in plant immunity and especially salicylic acid in shaping the root microbiome Lebeis et al 2015Plant roots exude a variety of compounds into the soil including carbohydrates amino acids and organic acids Jones 1998 Bais et al 2006 by diffusion ion channels and vesicular transport Bertin et al 2003 These compounds alter soil chemistry and provide nutrient sources for microbes in the rhizosphere Lynch and Whipps 1990 Bardgett et al 1998 Bever et al 2012 Miransari 2013 Studies with Arabidopsis barley maize potato or sugarcane revealed in addition to a soildependent variation a genotypedependent variation in the composition of the rhizosphere community Rasche et al 2006 Bulgarelli et al 2012 Lundberg et al 2012 Peiffer et al 2013 Bulgarelli et al 2015 Lebeis et al 2015 Yeoh et al 2015 These results are intriguing as it suggests a targeted restructuring of the rhizobiota by plants to serve their own benefits Further potato development slightly but significantly affected the rhizosphere community composition Rasche et al 2006 which is in accordance to Chaparro et al 2014 who observed plant developmentdependent changes in the composition of rhizobiomes that were associated with slight alterations in its metatranscriptome These findings might indicate a developmentspecific release of root exudates to establish microbiota activities that can enhance plant fitness Consistent with this wild oat roots showed root zonedependent difference in microbial communities with higher bacterial cell counts in the root tip and root hair zone as compared to bulk soil DeAngelis et al 2009 Consequently plants species can have different microbial communities associated with their roots This can lead to the selective enrichment of specific microbes along the root axis in the rhizosphere and support overall plant health and development Berendsen et al 2012 Moreover it might provide a source to use such plant–microbe interactions to identify heritable traits to improve crop productivity Mendes et al 2013 Peiffer et al 2013 or to select for microbiomes that can improve crop traits as has been reported for the genotypedriven selection for microbiomes that altered flowering in Arabidopsis thaliana and Brassica rapa PankeBuisse et al 2015

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