Abstract
Plants are hosts to complex communities of endophytic bacteria that colonize the interior of both below- and aboveground tissues. Bacteria living inside plant tissues as endophytes can be horizontally acquired from the environment with each new generation, or vertically transmitted from generation to generation via seed. A better understanding of bacterial endophyte transmission routes and modes will benefit studies of plant–endophyte interactions in both agricultural and natural ecosystems. In this review, we provide an overview of the transmission routes that bacteria can take to colonize plants, including vertically via seeds and pollen, and horizontally via soil, atmosphere, and insects. We discuss both well-documented and understudied transmission routes, and identify gaps in our knowledge on how bacteria reach the inside of plants. Where little knowledge is available on endophytes, we draw from studies on bacterial plant pathogens to discuss potential transmission routes. Colonization of roots from soil is the best studied transmission route, and probably the most important, although more studies of transmission to aerial parts and stomatal colonization are needed, as are studies that conclusively confirm vertical transfer. While vertical transfer of bacterial endophytes likely occurs, obligate and strictly vertically transferred symbioses with bacteria are probably unusual in plants. Instead, plants appear to benefit from the ability to respond to a changing environment by acquiring its endophytic microbiome anew with each generation, and over the lifetime of individuals.
Highlights
Plants are home to a myriad of microbes that live on below- and above-ground plant surfaces, called rhizosphere and phyllosphere, respectively
It is possible that some bacterial endophytes are transmitted both vertically and horizontally, and an endophyte that is beneficial to its host under a particular circumstance may be passed down to the offspring through the seed
It is conceivable that some plants may have formed mutualisms with bacteria that are vertically transmitted via seed, ensuring continued transmission of beneficial symbionts, similar to what has been described for defensive mutualisms between plants and fungal endophytes [68,69]
Summary
Plants are home to a myriad of microbes that live on below- and above-ground plant surfaces, called rhizosphere and phyllosphere, respectively. It is possible that some bacterial endophytes are transmitted both vertically and horizontally (i.e., mixed-mode transmission), and an endophyte that is beneficial to its host under a particular circumstance (e.g., biotic stress) may be passed down to the offspring through the seed. Vertical transmission of bacterial via seed and pollen likely occurs, as bacteria have been identified inside the seed of many different plant species (Figure 1A). Removal of rice seed endophytes by surface-sterilization and antibiotic treatments restricted seedling growth relative to control seedlings [49] Given such beneficial traits, it is conceivable that some plants may have formed mutualisms with bacteria that are vertically transmitted via seed, ensuring continued transmission of beneficial symbionts, similar to what has been described for defensive mutualisms between plants and fungal endophytes [68,69]. In Scots pine, in situ hybridization was used to detect endophytes in intact buds, where they were found to reside inside cells of scale primordia, meristems, and around the resin ducts buds [84]. rRNA abundance of these endophytes was quantified and found to be highest prior to growth or differentiation of the bud [93]
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