Brassinosteroids Regulate Plant Growth through Distinct Signaling Pathways in Selaginella and Arabidopsis

Abstract

Brassinosteroids (BRs) are growth-promoting steroid hormones that regulate diverse physiological processes in plants. Most BR biosynthetic enzymes belong to the cytochrome P450 (CYP) family. The gene encoding the ultimate step of BR biosynthesis in Arabidopsis likely evolved by gene duplication followed by functional specialization in a dicotyledonous plant-specific manner. To gain insight into the evolution of BRs, we performed a genomic reconstitution of Arabidopsis BR biosynthetic genes in an ancestral vascular plant, the lycophyte Selaginella moellendorffii. Selaginella contains four members of the CYP90 family that cluster together in the CYP85 clan. Similar to known BR biosynthetic genes, the Selaginella CYP90s exhibit eight or ten exons and Selaginella produces a putative BR biosynthetic intermediate. Therefore, we hypothesized that Selaginella CYP90 genes encode BR biosynthetic enzymes. In contrast to typical CYPs in Arabidopsis, Selaginella CYP90E2 and CYP90F1 do not possess amino-terminal signal peptides, suggesting that they do not localize to the endoplasmic reticulum. In addition, one of the three putative CYP reductases (CPRs) that is required for CYP enzyme function co-localized with CYP90E2 and CYP90F1. Treatments with a BR biosynthetic inhibitor, propiconazole, and epi-brassinolide resulted in greatly retarded and increased growth, respectively. This suggests that BRs promote growth in Selaginella, as they do in Arabidopsis. However, BR signaling occurs through different pathways than in Arabidopsis. A sequence homologous to the Arabidopsis BR receptor BRI1 was absent in Selaginella, but downstream components, including BIN2, BSU1, and BZR1, were present. Thus, the mechanism that initiates BR signaling in Selaginella seems to differ from that in Arabidopsis. Our findings suggest that the basic physiological roles of BRs as growth-promoting hormones are conserved in both lycophytes and Arabidopsis; however, different BR molecules and BRI1-based membrane receptor complexes evolved in these plants.

nana plant2 Encodes a Maize Ortholog of the Arabidopsis Brassinosteroid Biosynthesis Gene DWARF1, Identifying Developmental Interactions between Brassinosteroids and Gibberellins

“…Consistent with their role in forming structural sterols, such as sitosterol, genes encoding presumptive 24-sterol reductase activity are widely phylogenetically distributed in plants. In agreement with previous studies, we identified similar sequences in both Physcomitrella (Physcomitrella patens) and Selaginella (Mizutani and Ohta, 2010;Cheon et al, 2013;Hamberger and Bak, 2013). Physcomitrella and Selaginella each encode two paralogs that derive from duplication after the divergence of those lineages from each other and the remainder of the taxa (Supplemental Fig.…”

Functional Characterization of Soybean Glyma04g39610 as a Brassinosteroid Receptor Gene and Evolutionary Analysis of Soybean Brassinosteroid Receptors

“…This implies that the BR receptor complex evolved in a common ancestor of lycophytes, gymnosperms, and angiosperms. We found that a total of 67 BR receptors from dicots and monocots can be evolutionarily grouped into three clades represented by AtBRI1/OsBRI1, AtBRL1/OsBRL1, and AtBRL2/OsBRL2 with significant bootstrap support, which is in accordance with a previous study [ 72 ]. Each clade can be divided into two subclades, Ia, Ib, IIa, IIb, IIIa, and IIIb (100% bootstrap support), one subclade from monocots, and the other from dicots ( Figure 10 ).…”

“…Considering the existence of BRs in single-celled plants [ 64 ], we can not rule out the existence of BR receptor-like proteins in single-celled plants as some receptor kinase proteins might act as BR receptors. Interestingly, Cheon et al [ 72 ] reported that Selaginella lacks a homolog of AtBRI1, but does have downstream proteins such as BIN2, BSU1, and BZR1. This implies that the BR receptor complex evolved in a common ancestor of lycophytes, gymnosperms, and angiosperms.…”

Phosphorylation-dependent routing of RLP44 towards brassinosteroid or phytosulfokine signalling

“…This cell wall modification apparently evolved as an ancient cell wall consolidation mechanism and is operative in extant members of the charophycean green algae, which are the closest living relatives of land plants (Proseus and Boyer, 2006, Popper et al, 2011, Wolf et al, 2012a, Domozych et al, 2014, Nishiyama et al, 2018. On the other hand, it has been questioned whether BRI1-like brassinosteroid receptors are present in ancestral vascular plants (Cheon et al, 2013), thus RLP44 orthologues could predate some of its interaction partners. It will be interesting to dissect how a protein like RLP44, which modulates the function of distinct RLKs, co-evolved with its interaction partners.…”