Cross-kingdom signalling regulates spore germination in the moss Physcomitrella patens

Abstract

Plants live in close association with microorganisms that can have beneficial or detrimental effects. The activity of bacteria in association with flowering plants has been extensively analysed. Bacteria use quorum-sensing as a way of monitoring their population density and interacting with their environment. A key group of quorum sensing molecules in Gram-negative bacteria are the Nacylhomoserine lactones (AHLs), which are known to affect the growth and development of both flowering plants, including crops, and marine algae. Thus, AHLs have potentially important roles in agriculture and aquaculture. Nothing is known about the effects of AHLs on the earliest-diverging land plants, thus the evolution of AHL-mediated bacterial-plant/algal interactions is unknown. In this paper, we show that AHLs can affect spore germination in a representative of the earliest plants on land, the Bryophyte moss Physcomitrella patens. Furthermore, we demonstrate that sporophytes of some wild isolates of Physcomitrella patens are associated with AHL-producing bacteria. Plants do not exist in isolation in the environment, but interact with a wide array of organisms from all kingdoms including bacteria, fungi, animals and other plants. These interactions can have profound effects on plant fitness, growth and development. In addition to pathogenicity or parasitism, interactions between plants and other organisms can be beneficial. Examples include interactions between fungi and plants in the form of mycorrhizae and interactions between plants and bacteria 1-3. Interactions between plants and microorganisms have become more elaborate during plant evolution. Mycorrhizal interactions are beneficial in liverworts, one of the earliest diverging groups of land plants, where the association between liverworts and fungi boosts plant photosynthesis, growth, fitness and nitrogen/phosphorus uptake 4,5. In later-diverging plants including flowering plants, interactions with microorganisms have increased in complexity. For example, in legumes (Fabaceae, including beans and pulses) plant root cells are surrounded by a group of proteobacteria (Rhizobia) and form a symbiotic root nodule 6 while actinobacteria from the Frankia genus can form nodules with a wide range of plant families 7,8. The bacteria gain carbon from the plant, while the plant gains nitrogen from the bacteria. Not all plant-bacterial interactions are so highly specialised: many bacteria in the rhizosphere contribute to plant productivity and gain from plants in return 9. It has become clear that flowering plants can respond to bacterial signalling molecules that alter plant growth and development, representing inter-kingdom interaction 10,11. The perception of bacteria by plants is of significant importance in terms of monitoring their surroundings and thus being able to respond accordingly to enhance their chances of survival 12. A key way in which bacteria communicate with one another is via diffusible quorum sensing (QS) molecules that are used to monitor and respond to population d...

Axenic in vitro cultivation of 19 peat moss (Sphagnum L.) species as a resource for basic biology, biotechnology, and paludiculture

“…Differences in spore germination, plant development, and plant morphology between axenic moss cultures and field‐grown mosses may be due, besides obvious abiotic factors and speed of growth, to effects of the microbiome present only in the latter. Cross‐kingdom and cross‐clade signalling via small molecules can influence morphology of Sphagnum similar to P. patens (Kostka et al ., 2016; Decker et al ., 2017; Vesty et al ., 2020).…”

Harnessing intercellular signals to engineer the soil microbiome

“…49 Bacterial AHLs can both promote and downregulate sporulation of moss in a concentration-dependent manner. 50 Therefore, when considering optimising QS to benefit the plant in the microbiome, it is not simply a matter of inhibiting or quenching all signals.…”