bims-plasge 2019-12-08 papers

Issue of 2019–12–08
five papers selected by
Vera S. Bogdanova, ИЦиГ СО РАН

Trends Plant Sci. 2019 Nov 29. pii: S1360-1385(19)30278-X. [Epub ahead of print]

Unraveling the Linkage between Retrograde Signaling and RNA Metabolism in Plants.

Xiaobo Zhao, Jianyan Huang, Joanne Chory.

Retrograde signals are signals that originate in organelles to regulate nuclear gene expression. In plant cells, retrograde signaling from both chloroplasts and mitochondria is essential for plant development and growth. Over the past few years, substantial progress has been made in unraveling the linkages between chloroplast retrograde signaling and nuclear RNA metabolism processes or plastidial RNA editing. These findings add to the complexity of the regulation of organelle-to-nucleus communication. Chloroplast development and function rely on the coordinated regulation of chloroplast and nuclear gene expression, especially under stress conditions. A better understanding of retrograde signaling and RNA metabolism, as well as their connection, is essential for breeding stress-tolerant plants to cope with the dynamic and rapidly changing environment.

Keywords: RNA editing; RNA metabolism; alternative splicing; organelle; retrograde signaling

DOI: https://doi.org/10.1016/j.tplants.2019.10.009

J Plant Res. 2019 Dec 06.

Complex origins of chloroplast membranes with photosynthetic machineries: multiple transfers of genes from divergent organisms at different times or a single endosymbiotic event?

Naoki Sato.

The paradigm "cyanobacterial origin of chloroplasts" is currently viewed as an established fact. However, we may have to re-consider the origin of chloroplast membranes, because membranes are not replicated by their own. It is the genes for lipid biosynthetic enzymes that are inherited. In the current understandings, these enzymes became encoded by the nuclear genome as a result of endosymbiotic gene transfer from the endosymbiont. However, we previously showed that many enzymes involved in the synthesis of chloroplast peptidoglycan and glycolipids did not originate from cyanobacteria. Here I present results of comprehensive phylogenetic analysis of chloroplast enzymes involved in fatty acid and lipid biosynthesis, as well as additional chloroplast components related to photosynthesis and gene expression. Four types of phylogenetic relationship between chloroplast enzymes (encoded by the chloroplast and nuclear genomes) and cyanobacterial counterparts were found: type 1, chloroplast enzymes diverged from inside of cyanobacterial clade; type 2, chloroplast and cyanobacterial enzymes are sister groups; type 3, chloroplast enzymes originated from homologs of bacteria other than cyanobacteria; type 4, chloroplast enzymes diverged from eukaryotic homologs. Estimation of evolutionary distances suggested that the acquisition times of chloroplast enzymes were diverse, indicating that multiple gene transfers accounted for the chloroplast enzymes analyzed. Based on the results, I try to relax the tight logic of the endosymbiotic origin of chloroplasts involving a single endosymbiotic event by proposing alternative hypotheses. The hypothesis of host-directed chloroplast formation proposes that glycolipid synthesis ability had been acquired by the eukaryotic host before the acquisition of chloroplast ribosomes. Chloroplast membrane system could have been provided by the host, whereas cyanobacteria contributed to the genes for the genetic and photosynthesis systems, at various times, either before or after the formation of chloroplast membranes. The origin(s) of chloroplasts seems to be more complicated than the single event of primary endosymbiosis.

Keywords: Glycolipid biosynthesis; Hidden cyanobacterial lineage; Host-directed chloroplast formation; Membrane origin; Primary endosymbiosis

DOI: https://doi.org/10.1007/s10265-019-01157-z

Plant Mol Biol. 2019 Dec 03.

The dual-targeted RNA editing factor AEF1 is universally conserved among angiosperms and reveals only minor adaptations upon loss of its chloroplast or its mitochondrial target.

Anke Hein, Sarah Brenner, Monika Polsakiewicz, Volker Knoop.

KEY MESSAGE: Upon loss of either its chloroplast or mitochondrial target, a uniquely dual-targeted factor for C-to-U RNA editing in angiosperms reveals low evidence for improved molecular adaptation to its remaining target. RNA-binding pentatricopeptide repeat (PPR) proteins specifically recognize target sites for C-to-U RNA editing in the transcriptomes of plant chloroplasts and mitochondria. Among more than 80 PPR-type editing factors that have meantime been characterized, AEF1 (or MPR25) is a special case given its dual targeting to both organelles and addressing an essential mitochondrial (nad5eU1580SL) and an essential chloroplast (atpFeU92SL) RNA editing site in parallel in Arabidopsis. Here, we explored the angiosperm-wide conservation of AEF1 and its two organelle targets. Despite numerous independent losses of the chloroplast editing site by C-to-T conversion and at least four such conversions at the mitochondrial target site in other taxa, AEF1 remains consistently conserved in more than 120 sampled angiosperm genomes. Not a single case of simultaneous loss of the chloroplast and mitochondrial editing target or of AEF1 disintegration or loss could be identified, contrasting previous findings for editing factors targeted to only one organelle. Like in most RNA editing factors, the PPR array of AEF1 reveals potential for conceptually "improved fits" to its targets according to the current PPR-RNA binding code. Surprisingly, we observe only minor evidence for adaptation to the mitochondrial target also after deep losses of the chloroplast target among Asterales, Caryophyllales and Poales or, vice versa, for the remaining chloroplast target after a deep loss of the mitochondrial target among Malvales. The evolutionary observations support the notion that PPR-RNA mismatches may be essential for proper function of editing factors.

Keywords: Angiosperm phylogeny; C-to-U RNA editing; Dual organelle targeting; PPR-RNA recognition code; Plant chloroplasts and mitochondria; RNA-binding PPR proteins

DOI: https://doi.org/10.1007/s11103-019-00940-9

Front Plant Sci. 2019 ;10 1399

A Single Nucleotide Deletion in an ABC Transporter Gene Leads to a Dwarf Phenotype in Watermelon.

Huayu Zhu, Minjuan Zhang, Shouru Sun, Sen Yang, Jingxue Li, Hui Li, Huihui Yang, Kaige Zhang, Jianbin Hu, Dongming Liu, Luming Yang.

Dwarf habit is one of the most important traits in crop plant architecture, as it can increase plant density and improved land utilization, especially for protected cultivation, as well as increasing lodging resistance and economic yield. At least four dwarf genes have been identified in watermelon, but none of them has been cloned. In the current study, the Cldw-1 gene was primary-mapped onto watermelon chromosome 9 by next-generation sequencing-aided bulked-segregant analysis (BSA-seq) of F2 plants derived from a cross between a normal-height line, WT4, and a dwarf line, WM102, in watermelon. The candidate region identified by BSA-seq was subsequently validated and confirmed by linkage analysis using 30 simple sequence repeat (SSR) markers in an F2 population of 124 plants. The Cldw-1 gene was further fine-mapped by chromosome walking in a large F2 population of 1,053 plants and was delimited into a candidate region of 107.00 kb. Six genes were predicted to be in the candidate region, and only one gene, Cla010337, was identified to have two single nucleotide polymorphisms (SNPs) and a single nucleotide deletion in the exons in the dwarf line, WM102. A derived cleaved amplified polymorphic sequence (dCAPS) marker was developed from the single nucleotide deletion, co-segregated with the dwarf trait in both the F2 population and a germplasm collection of 165 accessions. Cla010337 encoded an ATP-binding cassette transporter (ABC transporter) protein, and the expression levels of Cla010337 were significantly reduced in all the tissues tested in the dwarf line, WM102. The results of this study will be useful in achieving a better understanding of the molecular mechanism of the dwarf plant trait in watermelon and for the development of marker-assisted selection (MAS) for new dwarf cultivars.

Keywords: ABC transporter; BSA-seq; SSR marker; dwarf; fine mapping; watermelon

DOI: https://doi.org/10.3389/fpls.2019.01399

Plant Physiol. 2019 Dec 02. pii: pp.01246.2019. [Epub ahead of print]

Non-catalytic subunits facilitate quaternary organization of plastidic acetyl-CoA carboxylase.

Kiran-Kumar Shivaiah, Geng Ding, Bryon Upton, Basil J Nikolau.

Arabidopsis (Arabidopsis thaliana), like most dicotyledonous plants, expresses a multicomponent, heteromeric acetyl-CoA carboxylase (htACCase), which catalyzes the generation of the malonyl-CoA precursor of de novo fatty acid biosynthesis. This enzyme consists of four catalytic subunits: biotin carboxylase (BC), carboxyltransferase (CT)-α, CT-β, and biotin carboxyl carrier protein (BCCP1 or BCCP2). By co-expressing combinations of components in a bacterial expression system, we demonstrate non-catalytic BADCs facilitate the assembly and activation of BCCP-BADC-BC subcomplexes catalyzing the bicarbonate-dependent hydrolysis of ATP, which is the first half-reaction catalyzed by the htACCase enzyme. Although BADC proteins do not directly impact formation of the CT-αβ subcomplex, the BADC-facilitated BCCP-BADC-BC subcomplex can more readily interact with the CT-αβ subcomplex to facilitate the generation of malonyl-CoA. The Arabidopsis genome encodes three BADC isoforms (BADC1, BADC2, BADC3), and BADC2 and BADC3 (rather than BADC1), in combination with BCCP1, best support this quaternary-structural organizational and catalytic activation of the htACCase enzyme. Physiological genetic studies validate these attributes as Arabidopsis double mutants singularly expressing BADC2, BADC3 or BADC1 present increasingly greater deleterious impacts on morphological and biochemical phenotypes. Specifically, plants expressing only BADC2 develop normally, plants only expressing BADC3 suffer a stunted root-growth phenotype, and plants expressing only BADC1 are embryo-lethal. The latter phenotype may also be associated with the distinct sub-organelle localization of BADC1 in plastids as compared to the localization of the other two BADC homologs. These finding can inspire novel strategies to improve the biological sources of fats and oils for dietary and industrial applications.

DOI: https://doi.org/10.1104/pp.19.01246