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Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation.

ABSTRACT: The colonization of land by plants was a key event in the evolution of life. Here we report the draft genome sequence of the filamentous terrestrial alga Klebsormidium flaccidum (Division Charophyta, Order Klebsormidiales) to elucidate the early transition step from aquatic algae to land plants. Comparison of the genome sequence with that of other algae and land plants demonstrate that K. flaccidum acquired many genes specific to land plants. We demonstrate that K. flaccidum indeed produces several plant hormones and homologues of some of the signalling intermediates required for hormone actions in higher plants. The K. flaccidum genome also encodes a primitive system to protect against the harmful effects of high-intensity light. The presence of these plant-related systems in K. flaccidum suggests that, during evolution, this alga acquired the fundamental machinery required for adaptation to terrestrial environments.

SUBMITTER: Hori K

PROVIDER: S-EPMC4052687 | biostudies-literature | 2014

REPOSITORIES: biostudies-literature

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Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation.

Hori Koichi K Maruyama Fumito F Fujisawa Takatomo T Togashi Tomoaki T Yamamoto Nozomi N Seo Mitsunori M Sato Syusei S Yamada Takuji T Mori Hiroshi H Tajima Naoyuki N Moriyama Takashi T Ikeuchi Masahiko M Watanabe Mai M Wada Hajime H Kobayashi Koichi K Saito Masakazu M Masuda Tatsuru T Sasaki-Sekimoto Yuko Y Mashiguchi Kiyoshi K Awai Koichiro K Shimojima Mie M Masuda Shinji S Iwai Masako M Nobusawa Takashi T Narise Takafumi T Kondo Satoshi S Saito Hikaru H Sato Ryoichi R Murakawa Masato M Ihara Yuta Y Oshima-Yamada Yui Y Ohtaka Kinuka K Satoh Masanori M Sonobe Kohei K Ishii Midori M Ohtani Ryosuke R Kanamori-Sato Miyu M Honoki Rina R Miyazaki Daichi D Mochizuki Hitoshi H Umetsu Jumpei J Higashi Kouichi K Shibata Daisuke D Kamiya Yuji Y Sato Naoki N Nakamura Yasukazu Y Tabata Satoshi S Ida Shigeru S Kurokawa Ken K Ohta Hiroyuki H

Nature communications 20140528

The colonization of land by plants was a key event in the evolution of life. Here we report the draft genome sequence of the filamentous terrestrial alga Klebsormidium flaccidum (Division Charophyta, Order Klebsormidiales) to elucidate the early transition step from aquatic algae to land plants. Comparison of the genome sequence with that of other algae and land plants demonstrate that K. flaccidum acquired many genes specific to land plants. We demonstrate that K. flaccidum indeed produces seve ...[more]

PMID: 24865297

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Project description:Main conclusionThe basal streptophyte Klebsormidium and the advanced Zygnema show adaptation to terrestrialization. Differences are found in photoprotection and resistance to short-term light changes, but not in CO 2 acquisition. Streptophyte green algae colonized land about 450-500 million years ago giving origin to terrestrial plants. We aim to understand how their physiological adaptations are linked to the ecological conditions (light, water and CO2) characterizing modern terrestrial habitats. A new Klebsormidium isolate from a strongly acidic environment of a former copper mine (Schwarzwand, Austria) is investigated, in comparison to Klebsormidium cf. flaccidum and Zygnema sp. We show that these genera possess different photosynthetic traits and water requirements. Particularly, the Klebsormidium species displayed a higher photoprotection capacity, concluded from non-photochemical quenching (NPQ) and higher tolerance to high light intensity than Zygnema. However, Klebsormidium suffered from photoinhibition when the light intensity in the environment increased rapidly, indicating that NPQ is involved in photoprotection against strong and stable irradiance. Klebsormidium was also highly resistant to cellular water loss (dehydration) under low light. On the other hand, exposure to relatively high light intensity during dehydration caused a harmful over-reduction of the electron transport chain, leading to PSII damages and impairing the ability to recover after rehydration. Thus, we suggest that dehydration is a selective force shaping the adaptation of this species towards low light. Contrary to the photosynthetic characteristics, the inorganic carbon (C i ) acquisition was equivalent between Klebsormidium and Zygnema. Despite their different habitats and restriction to hydro-terrestrial environment, the three organisms showed similar use of CO2 and HCO3- as source of Ci for photosynthesis, pointing out a similar adaptation of their CO2-concentrating mechanisms to terrestrial life.

Project description:BackgroundWalking catfish (Clarias batrachus) is a freshwater fish capable of air-breathing and locomotion on land. It usually inhabits various low-oxygen habitats, burrows inside the mudflat, and sometimes "walks" to search for suitable environments during summer. It has evolved accessory air-breathing organs for respiring air and corresponding mechanisms to survive in such challenging environments. Thereby, it serves as a great model for understanding adaptations to terrestrial life.ResultsComparative genomics with channel catfish (Ictalurus punctatus) revealed specific adaptations of C. batrachus in DNA repair, enzyme activator activity, and small GTPase regulator activity. Comparative analysis with 11 non-air-breathing fish species suggested adaptive evolution in gene expression and nitrogenous waste metabolic processes. Further, myoglobin, olfactory receptor related to class A G protein-coupled receptor 1, and sulfotransferase 6b1 genes were found to be expanded in the air-breathing walking catfish genome, with 15, 15, and 12 copies, respectively, compared to non-air-breathing fishes that possess only 1-2 copies of these genes. Additionally, we sequenced and compared the transcriptomes of the gill and the air-breathing organ to characterize the mechanism of aerial respiration involved in elastic fiber formation, oxygen binding and transport, angiogenesis, ion homeostasis and acid-base balance. The hemoglobin genes were expressed dramatically higher in the air-breathing organ than in the gill of walking catfish.ConclusionsThis study provides an important genomic resource for understanding the adaptive mechanisms of walking catfish to terrestrial environments. It is possible that the coupling of enhanced abilities for oxygen storage and oxygen transport through genomic expansion of myoglobin genes and transcriptomic up-regulation of hemoglobin and angiogenesis-related genes are important components of the molecular basis for adaptation of this aquatic species to terrestrial life.

Dataset Information

Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation.

Publications

Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation.

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