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New homologues of Brassicaceae water-soluble chlorophyll proteins shed light on chlorophyll binding, spectral tuning, and molecular evolution.

ABSTRACT: Type-II water-soluble chlorophyll (Chl) proteins (WSCPs) of Brassicaceae are promising models for understanding how protein sequence and structure affect Chl binding and spectral tuning in photosynthetic Chl-protein complexes. However, to date, their use has been limited by the small number of known WSCPs, which also limited understanding their physiological roles. To overcome these limitations, we performed a phylogenetic analysis to compile a more comprehensive and complete set of natural type-II WSCP homologues. The identified homologues were heterologously expressed in Escherichia coli, purified, tested for assembly with chlorophylls, and spectroscopically characterized. The analyses led to the discovery of previously unrecognized type-IIa and IIb subclass WSCPs, as well as of a new subclass that did not bind chlorophylls. Further analysis by ancestral sequence reconstruction yielded sequences of putative ancestors of the three subclasses, which were subsequently recombinantly expressed in E. coli, purified and characterized. Combining the phylogenetic and spectroscopic data with molecular structural information revealed distinct Chl-binding motifs, and identified residues critically impacting spectral tuning. The distinct Chl-binding properties of the WSCP archetypes suggest that the non-Chl-binding subclass evolved from a Chl-binding ancestor that most likely lost its Chl-binding capacity upon localization in the plant tissues with low Chl content. This dual evolutionary trajectory is consistent with WSCPs association with the Kunitz-type protease inhibitors superfamily, and indications of their inhibitory activity in response to various forms of stress in plants. These findings suggest new directions for exploring the physiological roles of WSCPs and the correlation, if any, between Chl-binding and protease inhibition functionality.

SUBMITTER: Prabahar V

PROVIDER: S-EPMC7054047 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Passiflora (passionflowers) makes an excellent model for studying plant evolutionary development. They are mostly perennial climbers that display axillary tendrils, which are believed to be modifications of the inflorescence. Passionflowers are also recognized by their unique flower features, such as the extra whorls of floral organs composed of corona filaments and membranes enclosing the nectary. Although some work on Passiflora organ ontogeny has been done, the developmental identity of both Passiflora tendrils and the corona is still controversial. Here, we combined ultrastructural analysis and expression patterns of the flower meristem and floral organ identity genes of the MADS-box AP1/FUL clade to reveal a possible role for these genes in the generation of evolutionary novelties in Passiflora. RESULTS:We followed the development of structures arising from the axillary meristem from juvenile to adult phase in P. edulis. We further assessed the expression pattern of P. edulis AP1/FUL homologues (PeAP1 and PeFUL), by RT-qPCR and in situ hybridization in several tissues, correlating it with the developmental stages of P. edulis. PeAP1 is expressed only in the reproductive stage, and it is highly expressed in tendrils and in flower meristems from the onset of their development. PeAP1 is also expressed in sepals, petals and in corona filaments, suggesting a novel role for PeAP1 in floral organ diversification. PeFUL presented a broad expression pattern in both vegetative and reproductive tissues, and it is also expressed in fruits. CONCLUSIONS:Our results provide new molecular insights into the morphological diversity in the genus Passiflora. Here, we bring new evidence that tendrils are part of the Passiflora inflorescence. This points to the convergence of similar developmental processes involving the recruitment of genes related to flower identity in the origin of tendrils in different plant families. The data obtained also support the hypothesis that the corona filaments are likely sui generis floral organs. Additionally, we provide an indication that PeFUL acts as a coordinator of passionfruit development.

Project description:BackgroundChlamydiae are obligate intracellular bacteria of protists, invertebrates and vertebrates, but have not been found to date in photosynthetic eukaryotes (algae and embryophytes). Genes of putative chlamydial origin, however, are present in significant numbers in sequenced genomes of photosynthetic eukaryotes. It has been suggested that such genes were acquired by an ancient horizontal gene transfer from Chlamydiae to the ancestor of photosynthetic eukaryotes. To further test this hypothesis, an extensive search for proteins of chlamydial origin was performed using several recently sequenced algal genomes and EST databases, and the proteins subjected to phylogenetic analyses.ResultsA total of 39 proteins of chlamydial origin were retrieved from the photosynthetic eukaryotes analyzed and their identity verified through phylogenetic analyses. The distribution of the chlamydial proteins among four groups of photosynthetic eukaryotes (Viridiplantae, Rhodoplantae, Glaucoplantae, Bacillariophyta) was complex suggesting multiple acquisitions and losses. Evidence is presented that all except one of the chlamydial genes originated from an ancient endosymbiosis of a chlamydial bacterium into the ancestor of the Plantae before their divergence into Viridiplantae, Rhodoplantae and Glaucoplantae, i.e. more than 1.1 BYA. The chlamydial proteins subsequently spread through secondary plastid endosymbioses to other eukaryotes. Of 20 chlamydial proteins recovered from the genomes of two Bacillariophyta, 10 were of rhodoplant, and 10 of viridiplant origin suggesting that they were acquired by two different secondary endosymbioses. Phylogenetic analyses of concatenated sequences demonstrated that the viridiplant secondary endosymbiosis likely occurred before the divergence of Chlorophyta and Streptophyta.ConclusionWe identified 39 proteins of chlamydial origin in photosynthetic eukaryotes signaling an ancient invasion of the ancestor of the Plantae by a chlamydial bacterium accompanied by horizontal gene transfer. Subsequently, chlamydial proteins spread through secondary endosymbioses to other eukaryotes. We conclude that intracellular chlamydiae likely persisted throughout the early history of the Plantae donating genes to their hosts that replaced their cyanobacterial/plastid homologs thus shaping early algal/plant evolution before they eventually vanished.

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New homologues of Brassicaceae water-soluble chlorophyll proteins shed light on chlorophyll binding, spectral tuning, and molecular evolution.

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