bims-plasge 2022-06-19 papers

on Plastid genes

Issue of 2022‒06‒19
eleven papers selected by
Vera S. Bogdanova
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences

The GENOMES UNCOUPLED1 protein has an ancient, highly conserved role but not in retrograde signalling.
Both metaxin and Tom20 together with two mitochondria-specific motifs support mitochondrial targeting of dual-targeting AtSufE1.
The Key to the Future Lies in the Past: Insights from Grain Legume Domestication and Improvement Should Inform Future Breeding Strategies.
Precise genetic mapping of Rf18(t), a new fertility restorer gene from 'Nipponbare' for wild abortive cytoplasmic male sterility in rice (Oryza sativa L.).
Genetic and transcriptomic dissection of an artificially induced paired spikelets mutant of wheat (Triticum aestivum L.).
Identification and characterization of the novel leaf rust resistance gene Lr81 in wheat.
Fine mapping of Rf2, a minor Restorer-of-fertility (Rf) gene for cytoplasmic male sterility in chili pepper G164 (Capsicum annuum L.).
Chromosome-level genome assemblies of four wild peach species provide insights into genome evolution and genetic basis of stress resistance.
GREEN FLUORESCENT PROTEIN variants with enhanced folding are more efficiently imported into chloroplasts.
The plastid-encoded protein Orf2971 is required for protein translocation and chloroplast quality control.
Plastid and mitochondrial phylogenomics reveal correlated substitution rate variation in Koenigia (Polygonoideae, Polygonaceae) and a reduced plastome for Koenigia delicatula including loss of all ndh genes.

New Phytol. 2022 Jun 16.

The GENOMES UNCOUPLED1 protein has an ancient, highly conserved role but not in retrograde signalling.

Suvi Honkanen, Ian Small.

  The pentatricopeptide repeat protein GENOMES UNCOUPLED1 (GUN1) is required for chloroplast-to-nucleus signalling when plastid translation becomes inhibited during chloroplast development in Arabidopsis thaliana, but its exact molecular function remains unknown. We analysed GUN1 sequences in land plants and streptophyte algae. We tested functional conservation by complementation of the Arabidopsis gun1 mutant with GUN1 genes from the streptophyte alga Coleochate orbicularis or the liverwort Marchantia polymorpha. We also analysed the transcriptomes of M. polymorpha gun1 knock-out mutant lines during chloroplast development. GUN1 evolved within the streptophyte algal ancestors of land plants and is highly conserved among land plants but missing from the Rafflesiaceae that lack chloroplast genomes. GUN1 genes from C. orbicularis and M. polymorpha suppress the cold-sensitive phenotype of the Arabidopsis gun1 mutant and restore typical retrograde responses to treatments with inhibitors of plastid translation, even though M. polymorpha responds very differently to such treatments. Our findings suggest that GUN1 is an ancient protein that evolved within the streptophyte algal ancestors of land plants before the first plants colonised land more than 470 million years ago. Its primary role is likely to be in chloroplast gene expression and its role in chloroplast retrograde signalling probably evolved more recently.

Keywords:  GUN1; chloroplast; evolution; gene expression; retrograde signaling; streptophyte

DOI:  https://doi.org/10.1111/nph.18318
J Integr Plant Biol. 2022 Jun 17.

Both metaxin and Tom20 together with two mitochondria-specific motifs support mitochondrial targeting of dual-targeting AtSufE1.

Seungjin Woo, Byeongho Moon, Inhwan Hwang.

  Plant cells have two endosymbiotic organelles, chloroplasts and mitochondria. These organelles perform specific functions that depend on organelle-specific proteins. The majority of chloroplast and mitochondrial proteins are specifically imported by the transit peptide and presequence, respectively. However, a significant number of proteins are also dually targeted to these two organelles. Currently, it is not fully understood how proteins are dually targeted to both chloroplasts and mitochondria. In this study, the mechanism underlying mitochondrial targeting of dual targeting AtSufE1 in Arabidopsis was elucidated. The N-terminal fragment containing 80 residues of AtSufE1 (AtSufE1N80) was sufficient to confer dual targeting of reporter protein, AtSufE1N80:GFP, in protoplasts. Two sequence motifs, two arginine residues at 15th and 21st positions, and amino acid (aa) sequence motif AKTLLLRPLK from the 31st to 40th aa position, were responsible for targeting to mitochondria a portion of reporter proteins amid of the chloroplast targeting. The sequence motif PSEVPFRRT from the 41st to 50th aa position constitutes a common motif for targeting to both chloroplasts and mitochondria. For mitochondrial import of AtSufE1:N80, Metaxin played a critical role. In addition, BiFC and protein pull-down experiments showed that AtSufE1N80 specifically interacts with import receptors, Metaxin and Tom20. The interaction of AtSufE1N80 with Metaxin was required for the interaction with Tom20. Based on these results, we propose that mitochondrial targeting of dual-targeting AtSufE1 is mediated by both mitochondria-specific and common sequence motifs in the signal sequence through the interaction with import receptors, Metaxin and Tom20, in a successive manner. This article is protected by copyright. All rights reserved.

Keywords:  AtSufE1; Tom20; chloroplasts; common motif; dual targeting; metaxin; mitochondria; mitochondria-specific motif

DOI:  https://doi.org/10.1111/jipb.13312
Plant Cell Physiol. 2022 Jun 17. pii: pcac086. [Epub ahead of print]

The Key to the Future Lies in the Past: Insights from Grain Legume Domestication and Improvement Should Inform Future Breeding Strategies.

Abhishek Bohra, Abha Tiwari, Parwinder Kaur, Showkat Ahmad Ganie, Ali Raza, Manish Roorkiwal, Reyazul Rouf Mir, Alisdair R Fernie, Petr Smýkal, Rajeev K Varshney.

  Crop domestication is a co-evolutionary process that has rendered plants and animals significantly dependent on human interventions for survival and propagation. Grain legumes have played an important role in the development of Neolithic agriculture some 12000 years ago. Despite being early companions of cereals in the origin and evolution of agriculture, the understanding of grain legume domestication has lagged behind to that of cereals. Adapting plants for human use has resulted in distinct morpho-physiological changes between the wild ancestors and domesticates, and this distinction has been focus of several studies aimed at understanding the domestication process and the genetic diversity bottlenecks created. Growing evidence from research on archaeological remains, combined with genetic analysis and the geographical distribution of wild forms has improved the resolution of the process of domestication, diversification and crop improvement. In this review, we first summarize the significance of legume wild relatives as reservoirs of novel genetic variation for crop breeding programs. We then describe key legume features, which evolved in response to anthropogenic activities. Here we highlight how whole genome sequencing and incorporation of omics-level data have expanded our capacity to monitor the genetic changes accompanying these processes. Finally, we present our perspective on alternative routes centred on de novo domestication and re-domestication to impart significant agronomic advance of novel crops over existing commodities. A finely resolved domestication history of grain legumes will uncover future breeding targets to develop modern cultivars enriched with alleles that improve yield, quality and stress tolerance.

Keywords:  Crop wild relatives; diversification; domestication; genes; grain legumes; selective sweeps

DOI:  https://doi.org/10.1093/pcp/pcac086
Theor Appl Genet. 2022 Jun 14.

Precise genetic mapping of Rf18(t), a new fertility restorer gene from 'Nipponbare' for wild abortive cytoplasmic male sterility in rice (Oryza sativa L.).

Honggen Zhang, Xixu Li, Zuopeng Xu, Zihao Wan, Ruixuan Wang, Xiangqiang Zhao, Geliang Tu, Guohua Liang, Minghong Gu, Shuzhu Tang.

KEY MESSAGE: We mapped Rf18(t), a Restorer-of-fertility gene for wild abortive cytoplasmic male sterility from the japonica maintainer 'Nipponbare', to chromosome 1. The best candidate gene, LOC_Os01g71320, is predicted to encode hexokinase. Three-line hybrid rice obtained through cytoplasmic male sterility (CMS) has helped increase the yield of rice globally, and the wild abortive (WA)-type cytoplasm from wild rice (Oryza rufipogon Griff.) is used widely in three-line indica hybrids. The identification and mapping of the Restorer-of-fertility (Rf) genes in maintainer lines aided in uncovering the genetic basis of fertility restoration of WA-type CMS and the development of WA-type hybrids. In this study, we identified a new Rf gene, Rf18(t), for WA-type CMS from the japonica maintainer line 'Nipponbare' using a chromosome segment substitution line population derived from a cross between the indica line 9311 and 'Nipponbare.' Using a substitution mapping strategy, Rf18(t) was delimited to a 48-kb chromosomal region flanked by molecular marker loci ID01M28791 and ID01M28845 on chromosome 1. By comparative sequence analyses, we propose that LOC_Os01g71320 is the most likely candidate gene for Rf18(t), and it is predicted to encode hexokinase. Furthermore, Rf18(t) was found to function in fertility restoration probably by a posttranscriptional mechanism and its function is dependent on the genetic background of 9311. These results broaden our knowledge on the mechanism of fertility restoration of WA-type CMS lines and will facilitate the development of WA-type rice hybrids.

DOI: https://doi.org/10.1007/s00122-022-04142-8
Theor Appl Genet. 2022 Jun 13.

Genetic and transcriptomic dissection of an artificially induced paired spikelets mutant of wheat (Triticum aestivum L.).

Juanyu Zhang, Yanyan Tang, Xi Pu, Xuebing Qiu, Jinhui Wang, Tao Li, Zhao Yang, Yao Zhou, Yuxiao Chang, Junjun Liang, Haili Zhang, Guangbing Deng, Hai Long.

KEY MESSAGE: Morphological, genetic and transcriptomic characterizations of an EMS-induced wheat paired spikelets (PS) mutant were performed. A novel qualitative locus WPS1 on chromosome 1D was identified. Grain yield of wheat is significantly associated with inflorescence or spike architecture. However, few genes related to wheat spike development have been identified and their underlying mechanisms are largely unknown. In this study, we characterized an ethyl methanesulfonate (EMS)-induced wheat mutant, wheat paired spikelets 1 (wps1). Unlike a single spikelet that usually develops at each node of rachis, a secondary spikelet appeared below the primary spikelet at most of the rachis nodes of wps1. The microscope observation showed that the secondary spikelet initiated later than the primary spikelet. Genetic analysis suggested that the PS of wps1 is controlled by a single dominant nuclear gene, designated WHEAT PAIRED SPIKELETS 1 (WPS1). Further RNA-seq based bulked segregant analysis and molecular marker mapping localized WPS1 in an interval of 208.18-220.92 Mb on the chromosome arm 1DL, which is different to known genes related to spike development in wheat. By using wheat omics data, TraesCS1D02G155200 encoding a HD-ZIP III transcription factor was considered as a strong candidate gene for WPS1. Transcriptomic analysis indicated that PS formation in wps1 is associated with auxin-related pathways and may be regulated by networks involving TB1, Ppd1, FT1, VRN1, etc. This study laid the solid foundation for further validation of the causal gene of WPS1 and explored its regulatory mechanism in PS formation and inflorescence development, which may benefit to kernel yield improvement of wheat based on optimization or design of spike architecture in the future.

DOI: https://doi.org/10.1007/s00122-022-04137-5
Theor Appl Genet. 2022 Jun 18.

Identification and characterization of the novel leaf rust resistance gene Lr81 in wheat.

Xiangyang Xu, James Kolmer, Genqiao Li, Chengcheng Tan, Brett F Carver, Ruolin Bian, Amy Bernardo, Guihua Bai.

KEY MESSAGE: The novel, leaf rust seedling resistance gene, Lr81, was identified in a Croatian breeding line and mapped to a genomic region of less than 100 Kb on chromosome 2AS. Leaf rust, caused by Puccinia triticina, is the most common and widespread rust disease in wheat. Races of Puccinia triticina evolve rapidly in the southern Great Plains of the USA, and leaf rust resistance genes often lose effectiveness shortly after deployment in wheat production. PI 470121, a wheat breeding line developed by the University of Zagreb in Croatia, showed high resistance to Puccinia triticina races collected from Oklahoma, suggesting that PI 470121 could be a leaf rust resistance source for the southern Great Plains of the USA. Genetic analysis based on an F2 population and F2:3 families derived from the cross PI 470121 × Stardust indicated that PI 470121 carries a dominant seedling resistance gene, designated as Lr81. Linkage mapping delimited Lr81 to a genomic region of 96,148 bp flanked by newly developed KASP markers Xstars-KASP320 and Xstars-KASP323 on the short arm of chromosome 2A, spanning 67,030,206-67,132,354 bp in the Chinese Spring reference assembly (IWGSC RefSeq v1.0). Deletion bin mapping assigned Lr81 to the terminal bin 2AS-0.78-1.00. Allelism tests indicated that Lr81 is a distinctive leaf rust resistance locus with the physical order Lr65-Lr17-Lr81. Marker-assisted selection based on a set of markers closely linked to leaf rust resistance genes in PI 470121 and Stardust enabled identification of a recombinant inbred line RIL92 carrying Lr81 only. Lr81 is a valuable leaf rust resistance source that can be rapidly introgressed into locally adapted cultivars using KASP markers Xstars-KASP320 and Xstars-KASP323.

DOI: https://doi.org/10.1007/s00122-022-04145-5
Theor Appl Genet. 2022 Jun 16.

Fine mapping of Rf2, a minor Restorer-of-fertility (Rf) gene for cytoplasmic male sterility in chili pepper G164 (Capsicum annuum L.).

Zhenghai Zhang, Dongliang An, Hailong Yu, Liuqing Sun, Yacong Cao, Baoxi Zhang, Lihao Wang.

KEY MESSAGE: Genome re-sequencing and recombination analyses identified Capana06g000193 as a strong candidate for the minor male fertility restoration locus Rf2 in chili pepper G164 harboring two dominant male fertility restoration genes. Male fertility restoration genes of chili pepper restorer line G164 (Capsicum annuum L.) were studied using molecular marker genotypes of an F2 population (7G) of G164 crossed with the cytoplasmic male sterility line 77013A. The ratio of sterile to fertile single plants in the F2 population was 1:15. This result indicates that chili pepper G164 has two dominant restoration genes, which we designated as Rf1 and Rf2. An individual plant recessive for Rf1 and heterozygous for Rf2, 7G-112 (rf1rf1Rf2rf2), was identified by molecular marker selection and genetic analysis, and a single Rf2 gene-segregating population with a 3:1 ratio of fertile to sterile plants was developed from the self-pollination of male fertile individuals of 77013A and 7G-112 hybrid progeny. Bulk segregant analysis of fertile and sterile pools from the segregating populations was used to genetically map Rf2 to a 3.1-Mb region on chromosome 6. Rf2 was further narrowed to a 179.3-kb interval through recombination analysis of molecular markers and obtained the most likely candidate gene, Capana06g000193.

DOI: https://doi.org/10.1007/s00122-022-04143-7
BMC Biol. 2022 Jun 13. 20(1): 139

Chromosome-level genome assemblies of four wild peach species provide insights into genome evolution and genetic basis of stress resistance.

Ke Cao, Zhen Peng, Xing Zhao, Yong Li, Kuozhan Liu, Pere Arus, Weichao Fang, Changwen Chen, Xinwei Wang, Jinlong Wu, Zhangjun Fei, Lirong Wang.

  BACKGROUND: Peach (Prunus persica) is an economically important stone fruit crop in Rosaceae and widely cultivated in temperate and subtropical regions, emerging as an excellent material to study the interaction between plant and environment. During its genus, there are four wild species of peach, all living in harsh environments. For example, one of the wild species, P. mira, originates from the Qinghai-Tibet Plateau (QTP) and exhibits strong cold/ultraviolet ray environmental adaptations. Although remarkable progresses in the gene discovery of fruit quality-related traits in peach using previous assembled genome were obtained, genomic basis of the response of these wild species to different geographical environments remains unclear.RESULTS: To uncover key genes regulating adaptability in different species and analyze the role of genetic variations in resistance formation, we performed de novo genome assembling of four wild relatives of peach (P. persica), P. mira, P. davidiana, P. kansuensis, and P. ferganensis and resequenced 175 peach varieties. The phylogenetic tree showed that the divergence time of P. mira and other wild relatives of peach was 11.5 million years ago, which was consistent with the drastic crustal movement of QTP. Abundant genetic variations were identified in four wild species when compared to P. persica, and the results showed that plant-pathogen interaction pathways were enriched in genes containing small insertions and deletions and copy number variations in all four wild relatives of peach. Then, the data were used to identify new genes and variations regulating resistance. For example, presence/absence variations which result from a hybridization event that occurred between P. mira and P. dulcis enhanced the resistance of their putative hybrid, P. davidiana. Using bulked segregant analysis, we located the nematode resistance locus of P. kansuensis in chromosome 2. Within the mapping region, a deletion in the promoter of one NBS-LRR gene was found to involve the resistance by regulating gene expression. Furthermore, combined with RNA-seq and selective sweeps analysis, we proposed that a deletion in the promoter of one CBF gene was essential for high-altitude adaptation of P. mira through increasing its resistance to low temperature.
CONCLUSIONS: In general, the reference genomes assembled in the study facilitate our understanding of resistance mechanism of perennial fruit crops, and provide valuable resources for future breeding and improvement.

Keywords:  Comparative genomics; High-altitude adaptation; Peach; Stress resistance

DOI:  https://doi.org/10.1186/s12915-022-01342-y
Plant Physiol. 2022 Jun 14. pii: kiac291. [Epub ahead of print]

GREEN FLUORESCENT PROTEIN variants with enhanced folding are more efficiently imported into chloroplasts.

Jinseung Jeong, Byeongho Moon, Inhwan Hwang, Dong Wook Lee.

Chloroplasts and mitochondria are subcellular organelles that evolved from cyanobacteria and α-proteobacteria, respectively. Although they have their own genomes, the majority of their proteins are encoded by nuclear genes, translated by cytosolic ribosomes, and imported via outer and inner membrane translocon complexes. The unfolding of mature regions of proteins is thought to be a prerequisite for the import of the proteins into these organelles. However, it is not fully understood how protein folding properties affect their import into these organelles. In this study, we examined the import behavior of chloroplast and mitochondrial reporters with normal green fluorescent protein (GFP) and two GFP variants with enhanced folding propensity, superfolder GFP (sfGFP) and extra-superfolder GFP (esGFP), which is folded better than sfGFP. sfGFP and esGFP were less dependent on the sequence motifs of the transit peptide (TP) and import machinery during protein import into Arabidopsis (Arabidopsis thaliana) chloroplasts, compared to normal GFP. sfGFP and esGFP were efficiently imported into chloroplasts by a mutant TP with an alanine substitution in the N-terminal MLM motif, whereas the same mutant TP showed a defect in importing normal GFP into chloroplasts. Moreover, sfGFP and esGFP were efficiently imported into plastid protein import 2 (ppi2) and heat shock protein 93-V (hsp93-V) plants, which have mutations in atToc159 and Hsp93-V, respectively. In contrast, the presequence-mediated mitochondrial import of sfGFP and esGFP was severely impaired. Based on these results, we propose that the chloroplast import machinery is more tolerant to different folding states of preproteins, whereas the mitochondrial machinery is more specialized in the translocation of unfolded preproteins.

DOI: https://doi.org/10.1093/plphys/kiac291
Plant Cell. 2022 Jun 16. pii: koac180. [Epub ahead of print]

The plastid-encoded protein Orf2971 is required for protein translocation and chloroplast quality control.

Jiale Xing, Junting Pan, Heng Yi, Kang Lv, Qiuliang Gan, Meimei Wang, Haitao Ge, Xiahe Huang, Fang Huang, Yingchun Wang, Jean-David Rochaix, Wenqiang Yang.

Photosynthesis and the biosynthesis of many important metabolites occur in chloroplasts. In these semi-autonomous organelles, the chloroplast genome encodes approximately 100 proteins. The remaining chloroplast proteins, close to 3000, are encoded by nuclear genes whose products are translated in the cytosol and imported into chloroplasts. However, there is still no consensus on the composition of the protein import machinery including its motor proteins and on how newly imported chloroplast proteins are refolded. In this study, we have examined the function of orf2971, the largest chloroplast gene of Chlamydomonas reinhardtii. Depletion of Orf2971 causes accumulation of protein precursors, partial proteolysis and aggregation of proteins, increased expression of chaperones and proteases, and autophagy. Orf2971 interacts with the TIC complex, catalyzes ATP hydrolysis and associates with chaperones and chaperonins. We propose that Orf2971 is intimately connected to the protein import machinery and plays an important role in chloroplast protein quality control.

DOI: https://doi.org/10.1093/plcell/koac180
Mol Phylogenet Evol. 2022 Jun 08. pii: S1055-7903(22)00157-9. [Epub ahead of print]174 107544

Plastid and mitochondrial phylogenomics reveal correlated substitution rate variation in Koenigia (Polygonoideae, Polygonaceae) and a reduced plastome for Koenigia delicatula including loss of all ndh genes.

Xiao-Jian Qu, Xue-Jie Zhang, Dong-Ling Cao, Xiu-Xiu Guo, Jeffrey P Mower, Shou-Jin Fan.

  Koenigia, a genus proposed by Linnaeus, has a contentious taxonomic history. In particular, relationships among species and the circumscription of the genus relative to Aconogonon remain uncertain. To explore phylogenetic relationships of Koenigia with other members of tribe Persicarieae and to establish the timing of major evolutionary diversification events, genome skimming of organellar sequences was used to assemble plastomes and mitochondrial genes from 15 individuals representing 13 species. Most Persicarieae plastomes exhibit a conserved structure and content relative to other flowering plants. However, Koenigia delicatula has lost functional copies of all ndh genes and the intron from atpF. In addition, the rpl32 gene was relocated in the K. delicatula plastome, which likely occurred via overlapping inversions or differential expansion and contraction of the inverted repeat. The highly supported but conflicting relationships between plastome and mitochondrial trees and among gene trees complicates the circumscription of Koenigia, which could be caused by rapid diversification within a short period. Moreover, the plastome and mitochondrial trees revealed correlated variation in substitution rates among Persicarieae species, suggesting a shared underlying mechanism promoting evolutionary rate variation in both organellar genomes. The divergence of dwarf K. delicatula from other Koenigia species may be associated with the well-known Eocene Thermal Maximum 2 or Early Eocene Climatic Optimum event, while diversification of the core-Koenigia clade associates with the Mid-Miocene Climatic Optimum and the uplift of Qinghai-Tibetan Plateau and adjacent areas.

Keywords:  Evolutionary rate variation; Koenigia delicatula; Mitochondrial genes; Phylogenetics; Plastome structure; ndh gene loss

DOI:  https://doi.org/10.1016/j.ympev.2022.107544