Conservation of ethylene as a plant hormone over 450 million years of evolution

Abstract

Land plants evolved more than 450 million years ago from a lineage of freshwater charophyte green algae(1). The extent to which plant signalling systems existed before the evolutionary transition to land is unknown. Although charophytes occupy a key phylogenetic position for elucidating the origins of such signalling systems(2-4), there is a paucity of sequence data for these organisms(5,6). Here we carry out de novo transcriptomics of five representative charophyte species, and find putative homologues for the biosynthesis, transport, perception and signalling of major plant hormones. Focusing on the plant hormone ethylene, we provide evidence that the filamentous charophyte Spirogyra pratensis possesses an ethylene hormone system homologous to that in plants. Spirogyra produces ethylene and exhibits a cell elongation response to ethylene. Spirogyra ethylene-signalling homologues partially rescue mutants of the angiosperm Arabidopsis thaliana and respond post-translationally to ethylene when expressed in plant cells, indicative of unambiguously homologous ethylene-signalling pathways in Spirogyra and Arabidopsis. These findings imply that the common aquatic ancestor possessed this pathway prior to the colonization of land and that cell elongation was possibly an ancestral ethylene response. This highlights the importance of charophytes for investigating the origins of fundamental plant processes.

On plant defense signaling networks and early land plant evolution

“…[94,111-114]]; yet we are only beginning to understand the function of these phytohormones in streptophyte algae [115-117]. All three canonical plant defense phytohormones, JA, SA and ET, have been detected in at least some species of streptophyte algae [94,112,115,118]. They also have been explored with regard to pathogen defense in non-flowering land plants.…”

“…In streptophyte algae, Ju et al [112] detected Isochorismate Synthase 1 (ICS1) homologs; ICS1 catalyzes the first step in SA biosynthesis. Furthermore, an ortholog of phenylalanine ammonia lyase (PAL), the enzyme catalyzing the first step in the phenylpropanoid (PP) pathway, was detected in the genome of K. nitens [121].…”

“…Moreover, potential homologs for the SA receptor Nonexpressor of PR genes 1 (NPR1) [123], were reported for all land plants [113] and the putative NPR1 homolog of P. patens can partially complement defense signaling-associated phenotypes of the Arabidopsis npr1 mutant [124]. As for ET, recent studies showed that streptophyte algae produce, sense and respond to ET [112,115], but these studies did not dissect the role of ET as a hormone involved in defense.…”

“…The canonical pathway genes for JA biosynthesis (13-LOX, 13-Lipoxygenase; AOS, 13-Allene Oxide Synthase; AOC, Allene Oxide Cyclase, OPR3, OPDA Reductase 3 and JAR1, Jasmonate Resistant 1) are present in all land plant lineages [125], and some of its components were also detected in several streptophyte algae [94,112,125]. However, actual (mainly mass spectrometry-based) measurements of JA levels are suggestive of a patchier distribution among land plants and streptophyte algae.…”

Cloning and Identification of an ACO Gene Involved in Ethylene Production Pathway from Ginkgo biloba

“…A simplified overview of the pathway is presented in figure 1. The number of sequenced lower plant genomes has increased extensively in the past few years, providing opportunities to trace the evolutionary origins of biosynthetic and signaling pathways of plant hormones (Ross and Reid, 2010;Ju et al, 2015). The ethylene biosynthetic pathway, which includes three key enzymes reactions, has been well-documented in higher plants.…”