HTL/KAI2 signalling substitutes for light to control plant germination

Abstract

Deciphering signalling pathways is essential to understanding how organisms respond to environmental cues but elucidating how these signalling pathways evolve in new environments is less clear.1,2 Most plants, for example, monitor multiple environmental cues to optimize the time and place to germinate. Some root parasitic plants, however, germinate in response to small molecules like strigolactones (SLs) emanating from host roots3,4 whilst a number of ephemeral weeds germinate in response to chemicals called karrikins (KARs) released after a forest fire.5,6 Although these species represent distinct clades, they use the same HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE 2 (HTL/KAI2) signalling pathway to perceive strigolactones or karrikins, which suggests convergent evolution.3,5 Because specialist lifestyles are derived traits, it is not clear if HTL/KAI2 signalling in these species evolved from a specific germination-signalling pathway or whether this pathway had other functions that were co-opted for specialist germination circumstances. Here, we show HTL/KAI2 signalling in Arabidopsis bypasses the light requirement for germination. In part, this is because the HTL/KAI2 downstream component, SMAX1 impinges on PHYTOCHROME INTERACTING FACTOR 1/PHYTOCHROME INTERACTING FACTOR 3-LIKE 5 (PIF1/PIL5)-regulated hormone response pathways conducive to germination. We identified Arabidopsis accessions that can germinate in the dark, which had altered expression of HTL/KAI2 signalling components, suggesting that divergence in this signalling pathway occurs in nature. Moreover, Arabidopsis HTL/KAI2-regulated gene signatures were observed in germinating Striga seed. The ability of HTL/KAI2 signalling to substitute for light advances an explanation for how some specialist plants evolved their underground germination behaviour in response to specific environments.

The genetic basis of plants’ battle against witchweeds: linking immune responses to distinct resistance mechanisms

“…The Striga life cycle depends on host-derived signals: strigolactones trigger Striga seed germination ( Bouwmeester et al , 2007 ; Ejeta, 2007 ; Kountche et al , 2019 ; Bunsick et al , 2020 , 2022 , Preprint), while haustorium-inducing factors enable formation of the penetrative structure from the Striga radicle ( Bandaranayake et al , 2010 ). Each Striga plant produces up to 0.5 million seeds, which can remain viable in the soil for 20 years ( Yoneyama et al , 2010 ; David et al , 2022 ).…”

Karrikin perception and signalling

“…Events further downstream that link SMAX1/SMXL2 degradation to specific developmental outputs are gradually emerging and complex. For brevity, we will only note here that KAR/KL signalling integrates with light, temperature, auxin, ethylene, abscisic acid, brassinosteroid and gibberellin pathways (Nelson et al ., 2009, 2010; Waters & Smith, 2013; Wei et al ., 2016; Brun et al ., 2019; Bunsick et al ., 2020, 2022; Carbonnel et al ., 2020a; Bunsick & Lumba, 2021; Bursch et al ., 2021; Hamon‐Josse et al ., 2022; Kim et al ., 2022; Park et al ., 2022; Villaécija‐Aguilar et al ., 2022). This will be a rich area for future study.…”

“…Interestingly, DLK2 expression is also increased in response to root colonisation by AM fungi in tomato and rice (Ho‐Plágaro et al ., 2021; Sisaphaithong et al ., 2021). The function of DLK2 with regard to SCF MAX2 ‐dependent signalling is currently unclear (Végh et al ., 2017), but an Arabidopsis dlk2 mutant has shown reduced seed dormancy under light‐limited conditions, which could be consistent with increased KAR/KL signalling (Bunsick et al ., 2022). In tomato, DLK2 overexpression in roots reduces AM colonisation and inhibits arbuscule branching, whereas DLK2 silencing has the opposite effect.…”