Evolution of ethylene as an abiotic stress hormone in streptophytes

Abstract

All land plants modulate their growth and physiology through intricate signaling cascades. The majority of these are at least modulated-and often triggered-by phytohormones. Over the past decade, it has become apparent that some phytohormones have an evolutionary origin that runs deeper than plant terrestrialization-many emerged in the streptophyte algal progenitors of land plants. Ethylene is such a case. Here we synthesize the current knowledge on the evolution of the phytohormone ethylene and speculate about its deeply conserved role in adjusting stress responses of streptophytes for more than half a billion years of evolution.

Keywords: Abiotic stress; Ethylene; Phytohormones; Plant evolution; Plant physiology; Plant terrestrialization; Signaling cascades; Streptophyte algae.

Fig. 1

Streptophyte diversity and the evolution of ethylene signaling. The cladogram shows the phylogenetic relationship within the monophylum Streptophyta, consisting of the paraphyletic grade streptophyte algae (blue) and the land plants that are split into the non-vascular bryophytes (yellow) and vascular tracheophytes (red). Land plants (orange) form together with the three streptophyte algal classes Zygnematophyceae, Coleochaetophyceae, and Charophyceae the monophylum Phragmoplastophyta. Projected onto the cladogram is which genes of the ethylene biosynthesis and signaling machinery likely were present in which most recent common ancestor. The topology of the cladogram is based on (Wickett et al., 2014; One Thousand Plant Transcriptomes Initiative, 2019).

Fig. 2

Ethylene is produced through different biochemical pathways by different life forms (plants, fungi and bacteria). (A) Plant ethylene biosynthesis pathway using 1-aminocyclopropane-1-carboxylic acid (ACC) as substrate. (B) Bacterial and fungal ethylene biosynthesis pathway using 2-keto-4-methylthiobutyric acid (KMBA) as substrate. (C) Bacterial and fungal ethylene biosynthesis pathway using 2-oxoglutarate as substrate. (D) Anaerobic bacterial ethylene biosynthesis pathway using (2-methylthio)ethanol as substrate by methylthio-alkane reductase (marBHDK). (E) Bacterial ethylene biosynthesis pathway using carbon monoxide as substrate. Abbreviations: MTA, methylthio-adenosine; HCN, hydrogencyanide; CH₃SH, methanethiol.

Fig. 3

Overview of plant evolution and the crucial transition from an aquatic to a terrestrial lifestyle. Ancestors of fresh-water streptophyte algae conquered land roughly 500 million years ago after the acquirement of ethylene as a functional plant hormone (amongst others), to enable responses towards to a diversity of abiotic stressors inherent to this habitat change.

Fig. 4

The intricate and conserved relation between abiotic stress, ethylene and the plastid. Abiotic stress impacts plastid performance and photosynthesis, directly or indirectly through ethylene as an important growth regulator. The role of ethylene in steering plant photosynthesis in evolutionary distant species ranging from cyanobacteria to angiosperms suggests fine-tuning photosynthesis is one of ethylene’s prime function in plants. The plastid plays a central role in mediating both stress signaling and ethylene responses, a feature conserved throughout plant evolutionary history.