KAI2 regulates seedling development by mediating light-induced remodelling of auxin transport.

Photomorphogenic remodelling of seedling growth is a key developmental transition in the plant life cycle. The α/ß-hydrolase signalling protein KARRIKIN-INSENSITIVE2 (KAI2), a close homologue of the strigolactone receptor DWARF14 (D14), is involved in this process, but it is unclear how the effects of KAI2 on development are mediated. Here, using a combination of physiological, pharmacological, genetic and imaging approaches in Arabidopsis thaliana (Heynh.) we show that kai2 phenotypes arise because of a failure to downregulate auxin transport from the seedling shoot apex towards the root system, rather than a failure to respond to light per se. We demonstrate that KAI2 controls the light-induced remodelling of the PIN-mediated auxin transport system in seedlings, promoting a reduction in PIN7 abundance in older tissues, and an increase of PIN1/PIN2 abundance in the root meristem. We show that removing PIN3, PIN4 and PIN7 from kai2 mutants, or pharmacological inhibition of auxin transport and synthesis, is sufficient to suppress most kai2 seedling phenotypes. We conclude that KAI2 regulates seedling morphogenesis by its effects on the auxin transport system. We propose that KAI2 is not required for the light-mediated changes in PIN gene expression but is required for the appropriate changes in PIN protein abundance within cells.

SMAX1/SMXL2 regulate root and root hair development downstream of KAI2-mediated signalling in Arabidopsis.

Karrikins are smoke-derived compounds presumed to mimic endogenous signalling molecules (KAI2-ligand, KL), whose signalling pathway is closely related to that of strigolactones (SLs), important regulators of plant development. Both karrikins/KLs and SLs are perceived by closely related α/ß hydrolase receptors (KAI2 and D14 respectively), and signalling through both receptors requires the F-box protein MAX2. Furthermore, both pathways trigger proteasome-mediated degradation of related SMAX1-LIKE (SMXL) proteins, to influence development. It has previously been suggested in multiple studies that SLs are important regulators of root and root hair development in Arabidopsis, but these conclusions are based on phenotypes observed in the non-specific max2 mutants and by use of racemic-GR24, a mixture of stereoisomers that activates both D14 and KAI2 signalling pathways. Here, we demonstrate that the majority of the effects on Arabidopsis root development previously attributed to SL signalling are actually mediated by the KAI2 signalling pathway. Using mutants defective in SL or KL synthesis and/or perception, we show that KAI2-mediated signalling alone regulates root hair density and root hair length as well as root skewing, straightness and diameter, while both KAI2 and D14 pathways regulate lateral root density and epidermal cell length. We test the key hypothesis that KAI2 signals by a non-canonical receptor-target mechanism in the context of root development. Our results provide no evidence for this, and we instead show that all effects of KAI2 in the root can be explained by canonical SMAX1/SMXL2 activity. However, we do find evidence for non-canonical GR24 ligand-receptor interactions in D14/KAI2-mediated root hair development. Overall, our results demonstrate that the KAI2 signalling pathway is an important new regulator of root hair and root development in Arabidopsis and lay an important basis for research into a molecular understanding of how very similar and partially overlapping hormone signalling pathways regulate different phenotypic outputs.

Wheat plants sense substrate volume and root density to proactively modulate shoot growth.

Plants must carefully coordinate their growth and development with respect to prevailing environmental conditions. To do this, plants can use a range of nutritional and non-nutritional information that allows them to proactively modulate their growth to avoid resource limitations. As is well-known to gardeners and horticulturists alike, substrate volume strongly influences plant growth, and maybe a key source of non-nutritional information for plants. However, the mechanisms by which these substrate volume effects occur remain unclear. Here, we show that wheat plants proactively modulate their shoot growth with respect to substrate volume, independent of nutrient availability. We show that these effects occur in two phases; in the first phase, the dilution of a mobile 'substrate volume-sensing signal' (SVS) allows plants to match their shoot (but not root) growth to the total size of the substrate, irrespective of how much of this they can occupy with their roots. In the second phase, the dilution of a less mobile 'root density-sensing signal' (RDS) allows plants to match root growth to actual rooting volume, with corresponding effects on shoot growth. We show that the effects of soil volume and plant density are largely interchangeable and that plants may use both SVS and RDS to detect their neighbours and to integrate growth responses to both volume and the presence of neighbours. Our work demonstrates the remarkable ability of plants to make proactive decisions about their growth, and has implications for mitigating the effects of dense sowing of crops in agricultural practice.

Fellowship of the rings: a saga of strigolactones and other small signals.

Strigolactones are an important class of plant signalling molecule with both external rhizospheric and internal hormonal functions in flowering plants. The past decade has seen staggering progress in strigolactone biology, permitting highly detailed understanding of their signalling, synthesis and biological roles - or so it seems. However, phylogenetic analyses show that strigolactone signalling mediated by the D14-SCFMAX2 -SMXL7 complex is only one of a number of closely related signalling pathways, and is much less ubiquitous in land plants than might be expected. The existence of closely related pathways, such as the KAI2-SMAX1 module, challenges many of our assumptions about strigolactones, and in particular emphasises how little we understand about the specificity of strigolactone signalling with respect to related signalling pathways. In this review, we examine recent advances in strigolactone signalling, taking a holistic evolutionary view to identify the ambiguities and uncertainties in our understanding. We highlight that while we now have highly detailed molecular models for the core mechanism of D14-SMXL7 signalling, we still do not understand the ligand specificity of D14, the specificity of its interaction with SMXL7, nor the specificity of SMXL7 function. Our analysis therefore identifies key areas requiring further study.

Environmental strigolactone drives early growth responses to neighboring plants and soil volume in pea.

There has been a dramatic recent increase in the understanding of the mechanisms by which plants detect their neighbors,1 including by touch,2 reflected light,3 volatile organic chemicals, and root exudates.4,5 The importance of root exudates remains ill-defined because of confounding experimental variables6,7 and difficulties disentangling neighbor detection in shoot and roots.8-10 There is evidence that root exudates allow distinction between kin and non-kin neighbors,11-13 but identification of specific exudates that function in neighbor detection and/or kin recognition remain elusive.1 Strigolactones (SLs), which are exuded into the soil in significant quantities in flowering plants to promote recruitment of arbuscular mycorrhizal fungi (AMF),14 seem intuitive candidates to act as plant-plant signals, since they also act as hormones in plants,15-17 with dramatic effects on shoot growth18,19 and milder effects on root development.20 Here, using pea, we test whether SLs act as either cues or signals for neighbor detection. We show that peas detect neighbors early in the life cycle through their root systems, resulting in strong changes in shoot biomass and branching, and that this requires SL biosynthesis. We demonstrate that uptake and detection of SLs exuded by neighboring plants are needed for this early neighbor detection, and that plants that cannot exude SLs are outcompeted by neighboring plants and fail to adjust growth to their soil volume. We conclude that plants both exude SLs as signals to modulate neighbor growth and detect environmental SLs as a cue for neighbor presence; collectively, this allows plants to proactively adjust their shoot growth according to neighbor density.

KAI2 promotes Arabidopsis root hair elongation at low external phosphate by controlling local accumulation of AUX1 and PIN2.

Root hair (RH) growth to increase the absorptive root surface area is a key adaptation of plants to limiting phosphate availability in soils. Despite the importance of this trait, especially for seedling survival, little is known about the molecular events connecting phosphate starvation sensing and RH growth regulation. KARRIKIN INSENSITIVE2 (KAI2), an α/ß-hydrolase receptor of a yet-unknown plant hormone ("KAI2-ligand" [KL]), is required for RH elongation.1 KAI2 interacts with the F-box protein MORE AXILLIARY BRANCHING2 (MAX2) to target regulatory proteins of the SUPPRESSOR of MAX2 1 (SMAX1) family for degradation.2 Here, we demonstrate that Pi starvation increases KL signaling in Arabidopsis roots through transcriptional activation of KAI2 and MAX2. Both genes are required for RH elongation under these conditions, while smax1 smxl2 mutants have constitutively long RHs, even at high Pi availability. Attenuated RH elongation in kai2 mutants is explained by reduced shootward auxin transport from the root tip resulting in reduced auxin signaling in the RH zone, caused by an inability to increase localized accumulation of the auxin importer AUXIN TRANSPORTER PROTEIN1 (AUX1) and the auxin exporter PIN-FORMED2 (PIN2) upon Pi starvation. Consistent with AUX1 and PIN2 accumulation being mediated via ethylene signaling,3 expression of 1-AMINOCYCLOPROPANE-1-CARBOXYLATE SYNTHASE 7 (ACS7) is increased at low Pi in a KAI2-dependent manner, and treatment with an ethylene precursor restores RH elongation of acs7, but not of aux1 and pin2. Thus, KAI2 signaling is increased by phosphate starvation to trigger an ethylene- AUX1/PIN2-auxin cascade required for RH elongation.