Desiccation tolerance in streptophyte algae and the algae to land plant transition: evolution of LEA and MIP protein families within the Viridiplantae

Abstract

The present review summarizes the effects of desiccation in streptophyte green algae, as numerous experimental studies have been performed over the past decade particularly in the early branching streptophyte Klebsormidium sp. and the late branching Zygnema circumcarinatum. The latter genus gives its name to the Zygenmatophyceae, the sister group to land plants. For both organisms, transcriptomic investigations of desiccation stress are available, and illustrate a high variability in the stress response depending on the conditions and the strains used. However, overall, the responses of both organisms to desiccation stress are very similar to that of land plants. We highlight the evolution of two highly regulated protein families, the late embryogenesis abundant (LEA) proteins and the major intrinsic protein (MIP) family. Chlorophytes and streptophytes encode LEA4 and LEA5, while LEA2 have so far only been found in streptophyte algae, indicating an evolutionary origin in this group. Within the MIP family, a high transcriptomic regulation of a tonoplast intrinsic protein (TIP) has been found for the first time outside the embryophytes in Z. circumcarinatum. The MIP family became more complex on the way to terrestrialization but simplified afterwards. These observations suggest a key role for water transport proteins in desiccation tolerance of streptophytes.

Keywords: Zygnema; Charophyta; LEA; MIP; Streptophyta; late embryogenesis abundant protein; major intrinsic protein; terrestrialization; transcriptome.

Fig. 1.

Importance of plant terrestrialization. (A) Biomass distribution on earth according to Bar-On et al. (2018. (B) Change in the atmospheric oxygen level during earth history. Reprinted by permission from Springer Nature. Lyons et al. (2014). The rise of oxygen in Earth’s early ocean and atmosphere. Nature 506, 307–315. Copyright 2014. Broken lines: alternative scenarios; GO, great oxygenation event. Possible ages for eukaroytes, primary plastids, and plant terrestrialization are indicated. (C) Chara vulgaris a representative of the Charophycae, which has often been suggested to be the sister of land plants. Zygnema circumcarinatum and Micrasterias crux-melitensis represent the filament and unicell life forms of the Zygnematophyceae, the sister clade to land plants. Image of Micrasterias crux-melitensis courtesy of Dr Monika Engels, Hamburg; with permission.

Fig. 2.

Effects of desiccation in Z. circumcarinatum. (A) Young filaments (1 month); young filament desiccated at 86% RH for 2 h (right), (B) old filaments (1 year); old filament desiccated at 86% RH for 2 h (right), scale bars=10 µm, (C) young filaments desiccated without or with pectate lyase (–/+PL), (D) old filaments desiccated without or with pectate lyase (–/+PL). Note the different time spans needed until the effective quantum yield dropped to zero. (C and D) are after Herburger et al. (2019).

Fig. 3.

Overall changes of gene expression levels in different Klebsormidium species and Zygnema circumcarinatum. Left (greenish) bars: number of up-regulated transcripts. Right (reddish) bars: number of down-regulated transcripts. The Klebsormidium experiments were performed at either 5 °C or 20 °C (data from Holzinger et al., 2014; Rippin et al., 2019a). For Z. circumcarinatum, the type of cultivation (L, liquid culture, 1 month old; P2 agar plate culture, 7 months old) is indicated (data from Rippin et al., 2017). The temperature in the Z. circumcarinatum experiment was 20 °C.

Fig. 4.

Phylogeny of MIPs within streptophytes: 78 protein sequences obtained from seven completed streptophyte genomes were analyzed using the phylogenetic pipeline by ETE3 (www.genome.jp/tools/ete/). See Supplementary Table S1 for a complete list of all proteins aligned. Alignment was performed using Clustal Omega v1.2.1 with the default options (Sievers and Higgins, 2014). The resulting alignment was cleaned using the gappyout algorithm of trimAI v1.4.rev6 (Capella-Gutiérez et al., 2009). The best protein model was selected using NJ tree inference among LG, WAG, JTT, MtREV, Dayhoff, DCMut, RtREV, CpREV, VT, Blosum62, MtMam, MtArt, HIVw, and HIVb models using pmodeltest v1.4. An ML tree was inferred using RAxML v8.1.20 run with model PROTGAMMALGF and default parameters (Stamatakis, 2014). Branch supports were computed out of 100 bootstrapped trees. Boostraps ≥90 are indicated. In addition, a few bootstraps ≥50 within the HIP/TIP/PIP cluster are indicated.