NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss.

Xiaohua Jin,Ming-Tsair Chan,Tracey A Ruhlman,Robert K Jansen,John C Blazier,Yao-Ting Huang,Choun-Sea Lin,Jeremy Jw Chen,De-Chih Liao,Jin Zhang,Wan-Jung Chang,Ming-Che Shih

doi:10.1186/s12870-015-0484-7

Abstract

BackgroundKey innovations have facilitated novel niche utilization, such as the movement of the algal predecessors of land plants into terrestrial habitats where drastic fluctuations in light intensity, ultraviolet radiation and water limitation required a number of adaptations. The NDH (NADH dehydrogenase-like) complex of Viridiplantae plastids participates in adapting the photosynthetic response to environmental stress, suggesting its involvement in the transition to terrestrial habitats. Although relatively rare, the loss or pseudogenization of plastid NDH genes is widely distributed across diverse lineages of photoautotrophic seed plants and mutants/transgenics lacking NDH function demonstrate little difference from wild type under non-stressed conditions. This study analyzes large transcriptomic and genomic datasets to evaluate the persistence and loss of NDH expression across plants.ResultsNuclear expression profiles showed accretion of the NDH gene complement at key transitions in land plant evolution, such as the transition to land and at the base of the angiosperm lineage. While detection of transcripts for a selection of non-NDH, photosynthesis related proteins was independent of the state of NDH, coordinate, lineage-specific loss of plastid NDH genes and expression of nuclear-encoded NDH subunits was documented in Pinaceae, gnetophytes, Orchidaceae and Geraniales confirming the independent and complete loss of NDH in these diverse seed plant taxa.ConclusionThe broad phylogenetic distribution of NDH loss and the subtle phenotypes of mutants suggest that the NDH complex is of limited biological significance in contemporary plants. While NDH activity appears dispensable under favorable conditions, there were likely sufficiently frequent episodes of abiotic stress affecting terrestrial habitats to allow the retention of NDH activity. These findings reveal genetic factors influencing plant/environment interactions in a changing climate through 450 million years of land plant evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0484-7) contains supplementary material, which is available to authorized users.

Highlights

Key innovations have facilitated novel niche utilization, such as the movement of the algal predecessors of land plants into terrestrial habitats where drastic fluctuations in light intensity, ultraviolet radiation and water limitation required a number of adaptations
To evaluate the distribution and timing of changes in the Plastid NAD(P)H dehydrogenaselike complex (NDH) gene complement across land plants a subject database comprising nuclear transcriptomes of photoautotrophic Streptophyta species was queried with Arabidopsis NDH-related coding sequences and the results of the survey mapped in a phylogenetic context
Queries included constituents of each of the four major subunits containing nuclear proteins, the Light harvesting complex genes/proteins (Lhca) proteins involved in tethering NDH to photosystem I (PSI) during supercomplex formation, assembly and accessory proteins, ndhF transcription factor Sig4 and proteins involved in maturation and editing of NDH transcripts in plastids

Summary

Introduction

Key innovations have facilitated novel niche utilization, such as the movement of the algal predecessors of land plants into terrestrial habitats where drastic fluctuations in light intensity, ultraviolet radiation and water limitation required a number of adaptations. Key innovations have facilitated novel niche utilization, such as the movement of the algal predecessors of land plants into terrestrial habitats [1] where fluctuations in light intensity, ultraviolet radiation and water limitation required a number of adaptations [1,2]. Mechanisms that permitted more refined control of the During the light reactions of photosynthesis in cyanobacteria, algae and plants, photons excite pigment/ chlorophyll molecules in photosystem II (PSII) at the stromal face of the chloroplast thylakoid membrane. The resulting high pH differential across the thylakoid membrane induces non-photochemical quenching (NPQ) allowing the dissipation of excess electrons under potentially unfavorable growth conditions including fluctuating, high intensity light, low CO2 concentration or drought stress [6,7]

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Results

Conclusion