Modulation of fungal phosphate homeostasis by the plant hormone strigolactone.

Inter-kingdom communication through small molecules is essential to the coexistence of organisms in an ecosystem. In soil communities, the plant root is a nexus of interactions for a remarkable number of fungi and is a source of small-molecule plant hormones that shape fungal compositions. Although hormone signaling pathways are established in plants, how fungi perceive and respond to molecules is unclear because many plant-associated fungi are recalcitrant to experimentation. Here, we develop an approach using the model fungus, Saccharomyces cerevisiae, to elucidate mechanisms of fungal response to plant hormones. Two plant hormones, strigolactone and methyl jasmonate, produce unique transcript profiles in yeast, affecting phosphate and sugar metabolism, respectively. Genetic analysis in combination with structural studies suggests that SLs require the high-affinity transporter Pho84 to modulate phosphate homeostasis. The ability to study small-molecule plant hormones in a tractable genetic system should have utility in understanding fungal-plant interactions.

Three mutations repurpose a plant karrikin receptor to a strigolactone receptor.

Uncovering the basis of small-molecule hormone receptors' evolution is paramount to a complete understanding of how protein structure drives function. In plants, hormone receptors for strigolactones are well suited to evolutionary inquiries because closely related homologs have different ligand preferences. More importantly, because of facile plant transgenic systems, receptors can be swapped and quickly assessed functionally in vivo. Here, we show that only three mutations are required to turn the nonstrigolactone receptor, KAI2, into a receptor that recognizes the plant hormone strigolactone. This modified receptor still retains its native function to perceive KAI2 ligands. Our directed evolution studies indicate that only a few keystone mutations are required to increase receptor promiscuity of KAI2, which may have implications for strigolactone receptor evolution in parasitic plants.

ShHTL7 requires functional brassinosteroid signaling to initiate GA-independent germination.

In the model plant Arabidopsis thaliana, two mutually antagonistic hormones regulate germination: abscisic acid (ABA) which promotes dormancy and gibberellins (GA) which breaks dormancy. Mutants auxotrophic for or insensitive to GA do not germinate. However, changes in the signaling flux through other hormone pathways will permit GA-independent germination. These changes include increased brassinosteroid (BR) signaling and decreased ABA signaling. Recently, strigolactone (SL) was also shown to enable GA-independent germination, provided the seeds express the SL receptor ShHTL7 from the parasitic plant Striga hermonthica. Here we show that a mutation which reduces sensitivity to BR (bri1-6) prevents ShHTL7 from promoting GA-independent germination. Further, we show that neither ShHTL7 nor the constitutive karrikin signaling mutant smax1-2 confer insensitivity to ABA. These results suggest ShHTL7 requires functional BR perception to bypass the GA requirement for germination.

Plant hormone signaling: Is upside down right side up?

Since the early days of plant biology, small molecule hormones have held a central place in our understanding of development. A key feature of plant hormone action is the ability to regulate multiple developmental processes. Despite this pleiotropy, decades of genetic and molecular studies have shown that plant hormone signaling is often canalized through a core pathway. This raises the difficult question of how one signaling pathway produces different outputs in different tissues. Drawing on examples from gibberellin and strigolactone signaling pathways, we propose this conceptual problem arises from an upside-down perspective of hormone signaling. Recent studies have revealed hormone and core pathway-independent mechanisms of regulating downstream signaling components, which could explain multiple developmental responses to the same hormone.

SMAX1-dependent seed germination bypasses GA signalling in Arabidopsis and Striga.

Parasitic plant infestations dramatically reduce the yield of many major food crops of sub-Saharan Africa and pose a serious threat to food security on that continent1. The first committed step of a successful infestation is the germination of parasite seeds primarily in response to a group of related small-molecule hormones called strigolactones (SLs), which are emitted by host roots2. Despite the important role of SLs, it is not clear how host-derived SLs germinate parasitic plants. In contrast, gibberellins (GA) acts as the dominant hormone for stimulation of germination in non-parasitic plant species by inhibiting a set of DELLA repressors3. Here, we show that expression of SL receptors from the parasitic plant Striga hermonthica in the presence of SLs circumvents the GA requirement for germination of Arabidopsis thaliana seed. Striga receptors co-opt and enhance signalling through the HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE 2 (AtHTL/KAI2) pathway, which normally plays a rudimentary role in Arabidopsis seed germination4,5. AtHTL/KAI2 negatively controls the SUPPRESSOR OF MAX2 1 (SMAX1) protein5, and loss of SMAX1 function allows germination in the presence of DELLA repressors. Our data suggest that ligand-dependent inactivation of SMAX1 in Striga and Arabidopsis can bypass GA-dependent germination in these species.

Chemical genetics and strigolactone perception.

Strigolactones (SLs) are a collection of related small molecules that act as hormones in plant growth and development. Intriguingly, SLs also act as ecological communicators between plants and mycorrhizal fungi and between host plants and a collection of parasitic plant species. In the case of mycorrhizal fungi, SLs exude into the soil from host roots to attract fungal hyphae for a beneficial interaction. In the case of parasitic plants, however, root-exuded SLs cause dormant parasitic plant seeds to germinate, thereby allowing the resulting seedling to infect the host and withdraw nutrients. Because a laboratory-friendly model does not exist for parasitic plants, researchers are currently using information gleaned from model plants like Arabidopsis in combination with the chemical probes developed through chemical genetics to understand SL perception of parasitic plants. This work first shows that understanding SL signaling is useful in developing chemical probes that perturb SL perception. Second, it indicates that the chemical space available to probe SL signaling in both model and parasitic plants is sizeable. Because these parasitic pests represent a major concern for food insecurity in the developing world, there is great need for chemical approaches to uncover novel lead compounds that perturb parasitic plant infections.