Transcriptome Profiling of the Green Alga Spirogyra pratensis (Charophyta) Suggests an Ancestral Role for Ethylene in Cell Wall Metabolism, Photosynthesis, and Abiotic Stress Responses

Abstract

It is well known that ethylene regulates a diverse set of developmental and stress-related processes in angiosperms, yet its roles in early-diverging embryophytes and algae are poorly understood. Recently, it was shown that ethylene functions as a hormone in the charophyte green alga Spirogyra pratensis. Since land plants evolved from charophytes, this implies conservation of ethylene as a hormone in green plants for at least 450 million years. However, the physiological role of ethylene in charophyte algae has remained unknown. To gain insight into ethylene responses in Spirogyra, we used mRNA sequencing to measure changes in gene expression over time in Spirogyra filaments in response to an ethylene treatment. Our analyses show that at the transcriptional level, ethylene predominantly regulates three processes in Spirogyra: (1) modification of the cell wall matrix by expansins and xyloglucan endotransglucosylases/hydrolases, (2) down-regulation of chlorophyll biosynthesis and photosynthesis, and (3) activation of abiotic stress responses. We confirmed that the photosynthetic capacity and chlorophyll content were reduced by an ethylene treatment and that several abiotic stress conditions could stimulate cell elongation in an ethylene-dependent manner. We also found that the Spirogyra transcriptome harbors only 10 ethylene-responsive transcription factor (ERF) homologs, several of which are regulated by ethylene. These results provide an initial understanding of the hormonal responses induced by ethylene in Spirogyra and help to reconstruct the role of ethylene in ancestral charophytes prior to the origin of land plants.

Plant evolution: landmarks on the path to terrestrial life

“…The signaling pathways of land plants often depend on phytohormones. Phytohormone-mediated signaling (homologous to that of land plants) has been detected in various streptophyte algae (Delaux et al, 2012;Hori et al, 2014;Ju et al, 2015;Van de Poel et al, 2016;Ohtaka et al, 2017) and polar transport of the phytohormone auxin has been shown for both Klebsormidium and Chara (Boot et al, 2012;Ohtaka et al, 2017). Furthermore, comparative genomic investigations reveal that the land plant common ancestor possessed a complex gene expression regulatory network that utilized 47 out of the 48 transcription factor families known from modern-day land plants (Catarino et al, 2016).…”

On plant defense signaling networks and early land plant evolution

“…A series of recent studies have revealed the presence of homologs of plant hormone biosynthesis and signaling pathway genes and/or the presence of various phytohormones in streptophyte algae [e.g. [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].…”

“…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.…”

“…A 1969 study by Markham and Porter [155] reported on the presence of flavonoids in the charophyceae Nitella , highlighting the need to further investigate streptophyte algae with regard to the presence of these metabolites. It is noteworthy that Van de Poel and colleagues [115] found ET-dependent regulation of a homolog of TRANSPARENT TESTA 8 ( TT8 ) in the Zygnematophyceae Spirogyra pratensis ; TT8 is a known regulator of flavonoid biosynthesis [156]. A TT8 ortholog is also present in the dataset for the Coleochaetophyceae Coleochaete scutata [114], where it is induced by high light stress.…”

Ethylene Exerts Species-Specific and Age-Dependent Control of Photosynthesis

“…The role of 50 ethylene in controlling photosynthesis was first described by Kays and Pallas in 1980, who found that 51 the hormone reduces photosynthesis in peanut (Arachis hypogaea). This hormonal control seems to 52 be an ancient response in plants because ethylene downregulates photosynthesis in the charophyte 53 green algae Spirogyra pratensis, suggesting that the regulation of photosynthesis by ethylene is 54 likely conserved and predates the colonization of non-aquatic habits by plants (Ju et al, 2015;Van 55 de Poel et al, 2016). 56…”