An ancient and conserved function for Armadillo‐related proteins in the control of spore and seed germination by abscisic acid

Abstract

Summary Armadillo‐related proteins regulate development throughout eukaryotic kingdoms. In the flowering plant Arabidopsis thaliana, Armadillo‐related ARABIDILLO proteins promote multicellular root branching. ARABIDILLO homologues exist throughout land plants, including early‐diverging species lacking true roots, suggesting that early‐evolving ARABIDILLOs had additional biological roles.Here we investigated, using molecular genetics, the conservation and diversification of ARABIDILLO protein function in plants separated by c. 450 million years of evolution.We demonstrate that ARABIDILLO homologues in the moss Physcomitrella patens regulate a previously undiscovered inhibitory effect of abscisic acid (ABA) on spore germination. Furthermore, we show that A. thaliana ARABIDILLOs function similarly during seed germination. Early‐diverging ARABIDILLO homologues from both P. patens and the lycophyte Selaginella moellendorffii can substitute for ARABIDILLO function during A. thaliana root development and seed germination.We conclude that (1) ABA was co‐opted early in plant evolution to regulate functionally analogous processes in spore‐ and seed‐producing plants and (2) plant ARABIDILLO germination functions were co‐opted early into both gametophyte and sporophyte, with a specific rooting function evolving later in the land plant lineage.

The decision to germinate is regulated by divergent molecular networks in spores and seeds

“…Our previous work suggested conservation of some hormone function in spore and seed germination, via an ABA-ARABIDILLO/PHYSCODILLO signalling module (Moody et al, 2016). Thus, we further explored the effects of diterpene hormones in Physcomitrella, to compare their effects with those of GAs in seeds.…”

“…The onset of germination in seeds is closely regulated by the balance between plant hormone signalling pathways of gibberellin (GA) and abscisic acid (ABA), which interact at multiple levels (Karssen & Lacka, 1986;Holdsworth et al, 2008a). We have recently shown that ABA inhibits spore germination in Physcomitrella and that conserved proteins modulate ABAmediated germination responses in both spores and seeds (Moody et al, 2016). This suggests that downstream signalling components regulating germination may be conserved between spores and angiosperm seeds.…”

What are the evolutionary origins of stomatal responses to abscisic acid in land plants?

“…Levels of ABA are controlled through the balanced regulation of key genes in the ABA biosynthesis and catabolism pathways (Qin and Zeevaart ; Kushiro et al ; Saito et al ). ABA can be found synthesized in all plants, from algae through to angiosperms, where it acts as a signaling molecule to control a variety of different plant processes, including growth, sex determination, seed/spore dormancy and stress tolerance (Hartung ; Takezawa et al ; Kobayashi et al ; McAdam et al ; Moody et al ). Accordingly, ABA‐signaling genes and associated transcriptional networks are conserved between angiosperms and extant representatives of the earliest land plant clades, even those which lack stomata (Richardt et al ; Hauser et al ; Lind et al ).…”

Effects of green seaweed extract onArabidopsisearly development suggest roles for hormone signalling in plant responses to algal fertilisers

“…Plates were transferred to the growth room for 7-10 days and incubated at 22 ± 2°C with a 16-h-light photoperiod and light intensity of 120µmolm -2 s -1 . Germination was observed daily as in 121 . A seed was scored as germinated when its radicle had emerged from within the seed coat.…”

“…20 seeds were placed individually on the agar following a line across the top of the plate. The plates were sealed with Micropore tape (3M), taped together and incubated vertically in standard growth conditions as in 121 .…”