bims-plasge 2019-03-03 papers

on Plastid genes

Issue of 2019‒03‒03
nine papers selected by
Vera S. Bogdanova
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences

Transcriptional and Post-transcriptional Regulation of Organellar Gene Expression (OGE) and Its Roles in Plant Salt Tolerance.
A missense mutation of STERILE APETALA leads to female sterility in Chinese cabbage (Brassica campestris ssp. pekinensis).
PPR proteins - orchestrators of organelle RNA metabolism.
Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land.
Identifying Genome-Wide Sequence Variations and Candidate Genes Implicated in Self-Incompatibility by Resequencing Fragaria viridis.
Novel Cytonuclear Combinations Modify Arabidopsis thaliana Seed Physiology and Vigor.
Engineering of plastids to optimize the production of high-value metabolites and proteins.
Divergence of RNA editing among Arabidopsis species.
Genetic diversity and relationship between cultivated, weedy and wild rye species as revealed by chloroplast and mitochondrial DNA non-coding regions analysis.

Int J Mol Sci. 2019 Feb 28. pii: E1056. [Epub ahead of print]20(5):

Transcriptional and Post-transcriptional Regulation of Organellar Gene Expression (OGE) and Its Roles in Plant Salt Tolerance.

Pedro Robles, Víctor Quesada.

  Given their endosymbiotic origin, chloroplasts and mitochondria genomes harbor only between 100 and 200 genes that encode the proteins involved in organellar gene expression (OGE), photosynthesis, and the electron transport chain. However, as the activity of these organelles also needs a few thousand proteins encoded by the nuclear genome, a close coordination of the gene expression between the nucleus and organelles must exist. In line with this, OGE regulation is crucial for plant growth and development, and is achieved mainly through post-transcriptional mechanisms performed by nuclear genes. In this way, the nucleus controls the activity of organelles and these, in turn, transmit information about their functional state to the nucleus by modulating nuclear expression according to the organelles' physiological requirements. This adjusts organelle function to plant physiological, developmental, or growth demands. Therefore, OGE must appropriately respond to both the endogenous signals and exogenous environmental cues that can jeopardize plant survival. As sessile organisms, plants have to respond to adverse conditions to acclimate and adapt to them. Salinity is a major abiotic stress that negatively affects plant development and growth, disrupts chloroplast and mitochondria function, and leads to reduced yields. Information on the effects that the disturbance of the OGE function has on plant tolerance to salinity is still quite fragmented. Nonetheless, many plant mutants which display altered responses to salinity have been characterized in recent years, and interestingly, several are affected in nuclear genes encoding organelle-localized proteins that regulate the expression of organelle genes. These results strongly support a link between OGE and plant salt tolerance, likely through retrograde signaling. Our review analyzes recent findings on the OGE functions required by plants to respond and tolerate salinity, and highlights the fundamental role that chloroplast and mitochondrion homeostasis plays in plant adaptation to salt stress.

Keywords:  Arabidopsis; DEAD-box RNA helicases (RHs)-containing proteins; PLASTID-SPECIFIC RIBOSOMAL PROTEIN 2; RNA-recognition motifs (RRMs)-containing proteins; SIGMA FACTOR 5; Salt stress; mitochondrial transcription termination factors (mTERFs); organellar gene expression (OGE); pentatricopeptide repeat (PPR) proteins; rice

DOI:  https://doi.org/10.3390/ijms20051056
Plant Reprod. 2019 Feb 26.

A missense mutation of STERILE APETALA leads to female sterility in Chinese cabbage (Brassica campestris ssp. pekinensis).

Wenjie Liu, Shengnan Huang, Zhiyong Liu, Tengxue Lou, Chong Tan, Yiheng Wang, Hui Feng.

  Flower development is essential for the sexual reproduction and crop yield of plants. Thus, a better understanding of plant sterility from the perspective of morphological and molecular genetics is imperative. In our previous study, a recessive female-sterile Chinese cabbage mutant fsm was obtained from a doubled haploid line 'FT' via an isolated microspore culture combined with EMS mutagenesis. Pistil aniline blue staining and stigma scanning observation showed that the growth of the stigma papillar cells and pollen tubes of the mutant fsm were normal. Therefore, the female sterility was due to abnormal development of the ovules. To map the mutant fsm, 3108 F2 individuals were selected for linkage analysis. Two closely linked markers, Indel-I2 and Indel-I7, were localized on the flanking region of fsm at distances of 0.05 cM and 0.06 cM, respectively. The physical distance between Indel-I2 and Indel-I7 was ~ 1376 kb, with 107 genes remaining in the target region. This region was located on the chromosome A04 centromere, on which low recombination rates and a high frequency of repetitive sequences were present. Whole-genome re-sequencing detected a single-nucleotide (C-to-A) transition (TCG/TAG) on the exon of BraA04001030, resulting in a premature stop codon. Genotyping revealed that the female-sterile phenotype was fully cosegregated with this SNP. BraA04001030 encodes a homologue of STERILE APETALA (SAP) transcriptional regulator, which plays vital roles in floral development. The results of the present study suggest that BraA04001030 is a strong candidate gene for fsm and provide the basis for exploring the molecular mechanism underlying female sterility in Chinese cabbage.

Keywords:  Chinese cabbage; EMS mutagenesis; Female-sterile; STERILE APETALA

DOI:  https://doi.org/10.1007/s00497-019-00368-7
Physiol Plant. 2019 Feb 27.

PPR proteins - orchestrators of organelle RNA metabolism.

Aleix Gorchs Rovira, Alison G Smith.

Pentatricopeptide repeat (PPR) proteins are important RNA regulators in chloroplasts and mitochondria, aiding in RNA editing, maturation, stabilisation or intron splicing, and in transcription and translation of organellar genes. In this review, we summarise all PPR proteins documented so far in plants and the green alga Chlamydomonas. By further analysis of the known target RNAs from Arabidopsis thaliana PPR proteins, we find that all organellar-encoded complexes are regulated by these proteins, although to differing extents. In particular, the orthologous complexes of NADH dehydrogenase (Complex I) in the mitochondria and NADH dehydrogenase-like (NDH) complex in the chloroplast were the most regulated, with respectively 60 and 28% of all characterised A. thaliana PPR proteins targeting their genes. This article is protected by copyright. All rights reserved.

DOI: https://doi.org/10.1111/ppl.12950
Proc Natl Acad Sci U S A. 2019 Feb 25. pii: 201812092. [Epub ahead of print]

Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land.

Chenchen Zhao, Yuanyuan Wang, Kai Xun Chan, D Blaine Marchant, Peter J Franks, David Randall, Estee E Tee, Guang Chen, Sunita Ramesh, Su Yin Phua, Ben Zhang, Adrian Hills, Fei Dai, Dawei Xue, Matthew Gilliham, Steve Tyerman, Eviatar Nevo, Feibo Wu, Guoping Zhang, Gane K-S Wong, James H Leebens-Mack, Michael Melkonian, Michael R Blatt, Pamela S Soltis, Douglas E Soltis, Barry J Pogson, Zhong-Hua Chen.

  Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3'-phosphoadenosine-5'-phosphate (PAP) metabolism, evolved in streptophyte algae-the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii, and the moss Physcomitrella patens Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these diverse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.

Keywords:  comparative genomics; green plant evolution; signal transduction; stomata; water stress

DOI:  https://doi.org/10.1073/pnas.1812092116
Int J Mol Sci. 2019 Feb 27. pii: E1039. [Epub ahead of print]20(5):

Identifying Genome-Wide Sequence Variations and Candidate Genes Implicated in Self-Incompatibility by Resequencing Fragaria viridis.

Jianke Du, Yan Lv, Jinsong Xiong, Chunfeng Ge, Shahid Iqbal, Yushan Qiao.

  It is clear that the incompatibility system in Fragaria is gametophytic, however, the genetic mechanism behind this remains elusive. Eleven second-generation lines of Fragaria viridis with different compatibility were obtained by manual self-pollination, which can be displayed directly by the level of fruit-set rate. We sequenced two second-generation selfing lines with large differences in fruit-set rate: Ls-S₂-53 as a self-incompatible sequencing sample, and Ls-S₂-76 as a strong self-compatible sequencing sample. Fragaria vesca was used as a completely self-compatible reference sample, and the genome-wide variations were identified and subsequently annotated. The distribution of polymorphisms is similar on each chromosome between the two sequencing samples, however, the distribution regions and the number of homozygous variations are inconsistent. Expression pattern analysis showed that six candidate genes were significantly associated with self-incompatibility. Using F. vesca as a reference, we focused our attention on the gene FIP2-like (FH protein interacting protein), associated with actin cytoskeleton formation, as the resulting proteins in Ls-S₂-53 and Ls-S₂-76 have each lost a number of different amino acids. Suppression of FIP2-like to some extent inhibits germination of pollen grains and growth of pollen tubes by reducing F-actin of the pollen tube tips. Our results suggest that the differential distribution of homozygous variations affects F. viridis fruit-set rate and that the fully encoded FIP2-like can function normally to promote F-actin formation, while the new FIP2-like proteins with shortened amino acid sequences have influenced the (in)compatibility of two selfing lines of F. viridis.

Keywords:  FIP2-like; Fragaria viridis; genome; resequencing; self-incompatibility; variations

DOI:  https://doi.org/10.3390/ijms20051039
Front Plant Sci. 2019 ;10 32

Novel Cytonuclear Combinations Modify Arabidopsis thaliana Seed Physiology and Vigor.

Clément Boussardon, Marie-Laure Martin-Magniette, Béatrice Godin, Abdelilah Benamar, Benjamin Vittrant, Sylvie Citerne, Tristan Mary-Huard, David Macherel, Loïc Rajjou, Françoise Budar.

  Dormancy and germination vigor are complex traits of primary importance for adaptation and agriculture. Intraspecific variation in cytoplasmic genomes and cytonuclear interactions were previously reported to affect germination in Arabidopsis using novel cytonuclear combinations that disrupt co-adaptation between natural variants of nuclear and cytoplasmic genomes. However, specific aspects of dormancy and germination vigor were not thoroughly explored, nor the parental contributions to the genetic effects. Here, we specifically assessed dormancy, germination performance and longevity of seeds from Arabidopsis plants with natural and new genomic compositions. All three traits were modified by cytonuclear reshuffling. Both depth and release rate of dormancy could be modified by a changing of cytoplasm. Significant changes on dormancy and germination performance due to specific cytonuclear interacting combinations mainly occurred in opposite directions, consistent with the idea that a single physiological consequence of the new genetic combination affected both traits oppositely. However, this was not always the case. Interestingly, the ability of parental accessions to contribute to significant cytonuclear interactions modifying the germination phenotype was different depending on whether they provided the nuclear or cytoplasmic genetic compartment. The observed deleterious effects of novel cytonuclear combinations (in comparison with the nuclear parent) were consistent with a contribution of cytonuclear interactions to germination adaptive phenotypes. More surprisingly, we also observed favorable effects of novel cytonuclear combinations, suggesting suboptimal genetic combinations exist in natural populations for these traits. Reduced sensitivity to exogenous ABA and faster endogenous ABA decay during germination were observed in a novel cytonuclear combination that also exhibited enhanced longevity and better germination performance, compared to its natural nuclear parent. Taken together, our results strongly support that cytoplasmic genomes represent an additional resource of natural variation for breeding seed vigor traits.

Keywords:  cytolines; cytonuclear co-adaptation; cytonuclear interaction; dormancy; germination; seed longevity; seed vigor

DOI:  https://doi.org/10.3389/fpls.2019.00032
Curr Opin Biotechnol. 2019 Feb 21. pii: S0958-1669(18)30152-6. [Epub ahead of print]59 8-15

Engineering of plastids to optimize the production of high-value metabolites and proteins.

Poul Erik Jensen, Lars B Scharff.

Plastids are interesting targets for metabolic engineering using the tools of synthetic biology. Plastids carry their own genome, which can be manipulated genetically in many algae and plants. Incorporating foreign genes into the plastid genome offers valuable benefits, such as high-level foreign protein expression and the absence of gene silencing. Here, we review progress in bioengineering of chloroplasts to produce valuable metabolites and proteins. Various strategies for enhancing yields of desired products, including design of operons, fusion proteins for improved translational efficiency, protein scaffolding, metabolic channeling and storage, are described. Efforts to control plastid differentiation also offer promising ways of turning plastids into controllable bio-factories, and the construction of synthetic plastids optimized for specific functions would be a major advance.

DOI: https://doi.org/10.1016/j.copbio.2019.01.009
Plant Sci. 2019 Mar;pii: S0168-9452(18)31002-1. [Epub ahead of print]280 241-247

Divergence of RNA editing among Arabidopsis species.

Akira Kawabe, Hazuka Y Furihata, Yudai Tsujino, Takahiro Kawanabe, Sota Fujii, Takanori Yoshida.

  RNA editing altered the RNA sequence by replacing the C nucleotide to U in the organellar genomes of plants. RNA editing status sometimes differed among distant species. The pattern of conservation and variation of RNA editing status made it possible to evaluate evolutionary mechanisms impacting functional aspects of RNA editing. In this study, divergence of RNA editing in the chloroplast genome among Arabidopsis species was analyzed to determine 9 losses and 1 gain in RNA editing. All changes in A. thaliana lineage resulted from changes to the chloroplast genome sequence, whereas changes in the A. lyrata / halleri lineage were possibly due to exclusive changes in the nuclear editing factors. One loss of RNA editing in A. lyrata was caused by a deficiency in the PPR gene OTP80. The changes in RNA editing occurred approximately every two million years and were not observed at functionally important sites. These results highlight the conserved nature of RNA editing status suggesting the importance of RNA editing during evolution.

Keywords:  Arabidopsis lyrata; Arabidopsis thaliana; Chloroplast; PPR; RNA editing

DOI:  https://doi.org/10.1016/j.plantsci.2018.12.009
PLoS One. 2019 ;14(2): e0213023

Genetic diversity and relationship between cultivated, weedy and wild rye species as revealed by chloroplast and mitochondrial DNA non-coding regions analysis.

Lidia Skuza, Izabela Szućko, Ewa Filip, Tomasz Strzała.

The genus Secale is small but very diverse. Despite the high economic importance, phylogenetic relationships of rye species have not been fully determined, and they are extremely important for the process of breeding of new cultivars that can be enriched with functional traits derived from wild rye species. The study analyzed the degree of relationship of 35 accessions of the genus Secale, representing 13 most often distinguished species and subspecies, originating from various seed collections in the world, based on the analysis of non-coding regions of the chloroplast (cpDNA) and mitochondrial genome (mtDNA), widely used in phylogenetic and population plant studies, because of a higher rate of evolution than the coding regions. There was no clear genetic structure between different species and subspecies, which may indicated the introgression between these taxa. The obtained data confirmed that S. vavilovii was very similar to S. cereale, which confirmed the assumption that they might share a common ancestor. The results also confirmed the divergence of S. sylvestre from other species and subspecies of rye. Areas that may be useful molecular markers in studies on closely related species of the genus Secale were also indicated.

DOI: https://doi.org/10.1371/journal.pone.0213023