Plant-associated microorganisms, such as bacteria and fungi, can grow on and survive in healthy plant tissues, making up the plant microbiome. Members of the plant microbiome can provide benefits to their host, and emerging research suggests that plants can reshape the composition of their microbiomes in response to environmental cues. The plant microbiome collectively acts as a reservoir for genes that may improve plant growth and survival in response to challenges, therefore contributing to the total genetic potential of the plant. Understanding the impact of the plant microbiome has unlocked new strategies for improving crop production, especially as climate change threatens to increase the prevalence of pathogens and stressful growth conditions. Applying microbiome engineering strategies, such as inoculation with plant growth-promoting rhizobacteria (PGPR), and incorporating the microbiome into the breeding process show promise for improving future agricultural crop production.
The plant microbiome expands the genetic potential of plants
Plants have evolved to form complex, beneficial relationships with the microorganisms in their surroundings. These plant-associated microorganisms can be found on a variety of tissues and collectively make up the plant microbiome. Although the plant microbiome includes bacteria, fungi, archaea, protists and viruses, the majority of research has focused on bacterial and fungal communities. The diverse communities of bacteria and fungi in the plant microbiome can have beneficial impacts on their hosts, such as improving growth, even when faced with challenges caused by biotic and abiotic stresses. Taking advantage of the benefits of the plant microbiome in agricultural practices could help enhance disease resistance, improve tolerance to abiotic stresses and reduce fertilizer usage.
Plants have a variety of organs that can be inhabited by microorganisms (Figure 1A). The rhizosphere, which is the root surface and nearby nutrient-rich soil environment that is affected by secreted exudates, is generally the niche with the highest abundance and species diversity. Estimates are that up to 20%–40% of plant photosynthate is secreted into the rhizosphere, making it one of the most nutrient-rich environments in the soil. Plant shoots and leaves, or the phyllosphere, can also harbour microbes, though usually fewer organisms are able to survive in these nutrient-poor and more exposed surfaces. A subset of specialized microorganisms can also colonize the inside of roots or shoots, known as the endosphere. The majority of microorganisms that form the plant microbiome originate from the surrounding soil or air (horizontal transmission) with a small subset inherited from the parent generation through seeds (vertical transmission).
The plant microbiome expands the genetic potential of plants. (a) Plant niches for microbes include the phyllosphere, rhizosphere and endosphere, the majority of which are horizontally acquired from the soil or air. Estimates for the number of colony-forming units (CFUs) and operational taxonomic units (OTUs), a metric of bacterial species diversity, are provided for each biological niche. (b) Collectively, the plant microbiome expands the plant’s potential to acquire nutrients, defend against pathogens and maintain nutrient homeostasis. Plant genomes range from ∼25,000 to 100,000 protein-encoding genes (e.g. Arabidopsis has ∼27,000 genes, tomato has ∼42,000 genes, rice has ∼40,000 genes and wheat has ∼100,000 genes). A single bacterial genome may encode 3000–8000 genes, and a typical plant supports 1000–10,000 bacterial OTUs. Although many bacterial strains encode genes with overlapping functions in their core genomes, strains within a single OTU may have up to 25% variation in their accessory genomes.
The sheer abundance and diversity of microorganisms in the plant microbiome allows it to make up a large reservoir of genes that can significantly impact plant fitness. The genes contributed to a plant’s genetic potential by the members of the plant microbiome can greatly outnumber the genes in the plant genome itself (Figure 1B). Plant genomes range from around 25,000 genes to 100,000 genes for the largest genomes like wheat. Bacterial genomes may range from 3000 to 8000 genes per genome. While many bacterial taxa have shared genetic content (their ‘core genomes’), the full collection of genes in a single genus (the pangenome) may exceed 15,000 genes, indicating that the genetic potential of thousands of microbes associated with a plant likely greatly exceeds the genetic potential of the plant. Since plants can shape their rhizosphere microbiome in response to stresses, plants can potentially harness the large functional diversity in their microbiomes for better adaptation to environmental conditions. Therefore, the genetic potential of the plant-associated microbiome should be taken into account when assessing the total genetic potential of a plant.
The composition of a plant’s microbiome is dynamic and can change over the course of a plant’s lifetime. Plant developmental stage, genotype and growth conditions can correlate with shifts in plant microbiome composition (Figure 2). For plants and other organisms, the core microbiome of a species is defined as the microbial taxa that associate as a result of evolutionary selection, though for some plants, the exact strains may vary between soils due to functional redundancy. In contrast, the accessory microbiome consists of the microorganisms that help plants adapt to their specific environmental condition. Additionally, rare taxa have been shown to have a larger contribution to microbiome functions than expected based on their abundance.
The microbiome composition changes in response to drought stress. Shown is the relative abundance of the most prevalent bacterial phyla in the sorghum rhizosphere microbiome (outer circle) and the changes in response to drought (inner circle). Using 16S rRNA amplicon sequencing data from a study performed by Xu et al. (2018), the bacterial composition of the rhizosphere microbiome of pre-flowering sorghum plants was compared under 8 weeks of well-watered versus drought conditions.
Mechanisms underlying microbially mediated benefits to plant health
Plants actively form beneficial relationships with microorganisms to help them grow and respond to challenges in their local environment. Beneficial bacteria that colonize the roots and rhizosphere are often called plant growth-promoting rhizobacteria (PGPR) because of their positive effect on plant health. Bacteria in the phyllosphere can induce plant immune responses and are known to play roles in pathogen protection. Plants can also form highly species-specific mutualistic interactions with microorganisms in the endosphere, such as nodule-forming bacteria and arbuscular mycorrhizal fungi, which can improve plant access to essential nutrients.
Associating with microorganisms can provide plants with novel genes and functions such as nutrient uptake and antimicrobial production. Plants require nitrogen to survive, but do not have genes that encode nitrogenase to convert atmospheric nitrogen into usable forms. A subset of plants has evolved symbiotic relations with nitrogen-fixing bacteria. For example, legumes can form nodules filled with nitrogen-fixing bacteria that provide the plant with a reliable source of nitrogen. While symbiotic nitrogen fixation has long been viewed as legume specific, plant-associated microbiomes are consistently enriched in bacteria that encode genes for nitrogen fixation. This suggests that many plants may receive a benefit from providing an ecological niche for microbial nitrogen fixation. Similarly, soil microorganisms can play an important role in increasing the availability of other essential nutrients to plants. Arbuscular mycorrhizal fungi can transport solubilized phosphorus and zinc into plant cells, whereas many PGPR can produce siderophores that increase iron availability for the plant. Some PGPR can produce unique antimicrobial or insecticidal compounds, conferring novel defence mechanisms against plant pathogens to the plant host. For example, some PGPR produce 2,4-diacetylphloroglucinol (DAPG), an antifungal agent that can target a broad range of pathogens.
Members of the plant microbiome can also provide plants with an adaptive advantage by modulating existing plant functions. Many beneficial microorganisms are capable of producing or degrading phytohormones, impacting plant hormone homeostasis with consequences for growth and development. For example, PGPR that synthesize auxin induce lateral root production, increasing the plant’s ability to take up water and nutrients. Some PGPR can produce 1-aminocyclopropane-1-carboxylate (ACC) deaminase, an enzyme that blocks plant ethylene biosynthesis in response to stress, and therefore prevents root stunting. The presence of certain bacteria can also prime the plant immune system for future attack from pathogens or insect herbivores. Furthermore, the plant microbiome can help reduce opportunities for pathogen infection through competitive exclusion, as pathogens must be able to outcompete existing microbiota for space and resources.
Harnessing the microbiome for agricultural improvement
Most agricultural practices do not consider the positive impact of microorganisms on plant growth. The majority of beneficial microorganisms that form the plant microbiome are recruited from the soil. However, current agricultural practices use a mixture of strategies that can drastically modify or harm the natural soil microbiota, impacting the diversity of microorganisms used to build the plant microbiome and creating dysbiotic soil systems. These strategies can include the use of pesticides, fertilizers or soil fumigation. In aeroponic or hydroponic systems, plants are grown without soil, losing access to a large source of beneficial microorganisms and potentially leaving them vulnerable to opportunistic pathogens. Therefore, enhancing the plant microbiome has a great potential to improve crop yields, especially as growing populations and climate change raise concerns for food security.
Gaps in current agricultural practices could potentially be filled by adding beneficial microbes into dysbiotic agriculture soils, thereby reintroducing beneficial genes to the plant. Researchers have discovered many PGPR that provide plants with an advantage under stressful conditions. In controlled lab and greenhouse experiments, the plant microbiome can be manipulated by introducing desirable PGPR strains, subsequently leading to improved plant growth under stress. However, there has been limited success when testing PGPR inoculants in agricultural soils. This may be because the introduced microbe is unable to outcompete existing microbes, adapt to the local soil environment, successfully colonize the plant or express the beneficial genes. The outcomes of these trials are highly dependent on the soil type, environmental conditions and plant genotype. So, even if a PGPR is successful in one field, it may not work in another.
Although the presence of certain members of the microbiome improves plant health, many of the genetic mechanisms for these processes are still unknown. In order to fully harness the genetic potential of the microbiome, it is essential to identify the underlying genetic and molecular mechanisms to translate this research for agricultural applications (Figure 3). For instance, having genetic markers for specific traits could help with screening for desirable PGPR that are adapted to a specific soil or plant. Alternatively, known beneficial microbial molecules can be purified and added to plants in lieu of conventional pesticides or fertilizers. This is currently done with Bt toxin, an insecticidal compound produced by the plant-associated microbe Bacillus thuringiensis. Knowing beneficial microbial genes can facilitate genetic engineering approaches to introduce beneficial microbial traits into plants. Finally, understanding what allows individual microbes to colonize specific plants, and how plants shape their associated communities, can guide breeding strategies.
The process of identifying genetic mechanisms behind plant growth-promoting traits in plant-associated microorganisms. An outline of an experimental process leading to the discovery of ACC deaminase, an enzyme that can promote plant growth under salinity stress. (a) Rhizobacteria are isolated from healthy maize growing in saline soil. (b) Isolated bacteria are each inoculated into the maize rhizosphere under saline conditions to identify strains that promote growth. (c) The beneficial bacterial strain (pink) is chemically mutagenized. The mutants (pink, patterned) are individually screened for a loss of protection against salt stress. (d) The mutant genome is sequenced and mapped to the wildtype genome. The causative mutation is confirmed by testing gene deletion mutants (pink, starred) under salt stress. (e) The gene encodes ACC deaminase (green), which cleaves ACC (purple and blue) into ammonia and α-ketobutyrate, upon binding.
By identifying the bacterial genes required to colonize specific plants and the plant genes required to shape their associated communities, microbiome engineering strategies could be applied during the breeding stage. Conventional breeding practices rely solely on variation in the plant genome to produce cultivars with desirable traits when challenged with pathogens or abiotic stresses. Over time, crops have been bred to grow in dysbiotic soil systems with lowered microbial diversity. This could lead to plants losing the ability to attract key members of the microbiome that could provide benefits in response to environmental stressors. However, incorporating the plant microbiome into breeding strategies introduces additional genetic variation that could be used to select for improvements in agronomically important traits. When breeding plants, it would be useful to propagate plants alongside key members of their microbiome, to help them maintain desirable plant–microbe interactions once introduced to their new environment (Figure 4). This starter microbiome could consist of a single PGPR inoculant, an artificial community of PGPR or microorganisms introduced from a soil sample13. However, it is difficult to design synthetic, interconnected communities consisting of desirable PGPR strains, without in-depth knowledge of the genetic mechanisms involved.
Overview of ways to incorporate microbiome engineering into agricultural cultivation practices. Microorganisms can be incorporated into the plant microbiome during the breeding stage, prior to large-scale cultivation. These microorganisms can be introduced by transplanting soils directly from the rhizosphere of healthy plants. Alternatively, the beneficial microorganisms in these soils can be analysed to identify PGPR. These PGPR can be formulated as a single PGPR inoculant, or as a synthetic community of PGPR, and introduced to plants during breeding.
Ideally, the microbiome could be modified to provide protection against a broad range of conditions, such as multiple abiotic stresses, pathogens and insect herbivores, in addition to maintaining or improving growth. However, all of these processes are intertwined and are often controlled by modulating levels of the same few hormones. This means that increased resistance in one area can come with trade-offs, such as increased sensitivity to another factor. For example, increased resistance to insects due to jasmonic acid production can come at a cost to salicylic acid-mediated defence against bacterial pathogens. Therefore, it would be more effective to develop microbial consortia to target the conditions of specific fields, on a case-by-case basis, rather than applying a generic consortium.
Future areas of research should include improving stable colonization of PGPR, untangling complex interactions between key microbes in a system and incorporating the plant microbiome into breeding strategies. Microbiome engineering could play a vital role in harnessing the genetic potential of the plant microbiome and prevent future crop loss due to abiotic stresses and pathogen infection.
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Nicole Wang is a MSc student in the Haney Lab at the University of British Columbia. She graduated from the University of Waterloo with a BSc in Biology. She studies the genetic mechanisms that allow beneficial bacteria in the rhizosphere to protect plants from root pathogens. Email: firstname.lastname@example.org
Cara Haney is an Assistant Professor at the University of British Columbia. She received her PhD from Stanford University and completed a post-doctoral fellowship at Harvard University. Her lab uses reductionist model systems combined with genetic and genomic approaches to identify the genes and molecular mechanisms that shape plant-microbiome interactions. Email: email@example.com