SnRK2 protein kinases represent an ancient system in plants for adaptation to a terrestrial environment

Akihisa Shinozawa,Yasuko Kamisugi,Yurie Hara,Ryoko Otake,Koichi Hori,Hiroyuki Ohta,Shinnosuke Ishikawa,Anna Amagai,Andrew C Cuming,Teruaki Taji,Yoichi Sakata,Fuminori Takahashi,Takahisa Hayashi,Taishi Umezawa,Kenji Komatsu,Keisuke Tanaka,Daisuke Takezawa,Kazuo Shinozaki

doi:10.1038/s42003-019-0281-1

Akihisa Shinozawa, Yasuko Kamisugi + Show 16 more

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https://doi.org/10.1038/s42003-019-0281-1

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The SNF1-related protein kinase 2 (SnRK2) family includes key regulators of osmostress and abscisic acid (ABA) responses in angiosperms and can be classified into three subclasses. Subclass III SnRK2s act in the ABA response while ABA-nonresponsive subclass I SnRK2s are regulated through osmostress. Here we report that an ancient subclass III SnRK2-based signalling module including ABA and an upstream Raf-like kinase (ARK) exclusively protects the moss Physcomitrella patens from drought. Subclass III SnRK2s from both Arabidopsis and from the semiterrestrial alga Klebsormidium nitens, which contains all the components of ABA signalling except ABA receptors, complement Physcomitrella snrk2− mutants, whereas Arabidopsis subclass I SnRK2 cannot. We propose that the earliest land plants developed the ABA/ARK/subclass III SnRK2 signalling module by recruiting ABA to regulate a pre-existing dehydration response and that subsequently a novel subclass I SnRK2 system evolved in vascular plants conferring osmostress protection independently from the ancient system.

Highlights

Due to their sessile nature, land plants have developed various strategies to cope with dehydration under waterdeficit conditions
Our results show the fundamental role of SnRK2 in ABA signalling as well as in osmostress and dehydration tolerance of P. patens, an extant member of a basal land plant lineage
We demonstrated that even an algal SnRK2 from the evolutionarily distant charophyte, K. nitens, is functionally equivalent to that of land plants in executing ABA signalling, clearly identifying that the origins of SnRK2-mediated responses predate the evolution of land plants

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Introduction

Due to their sessile nature, land plants have developed various strategies to cope with dehydration under waterdeficit conditions. PpOST1 results in defective ABA-responsive closure of moss stomata, which occur only at the base of sporophytes, the nondominant generation in bryophytes[14]. It is not known whether the Ppsnrk2a/Ppost[1] plant has a defect in the ABA responsiveness of the moss protonemata, where ABA responses as well as tolerance to desiccation and osmostress have been well documented[15,16,17,18,19]

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