bims-plasge 2019-03-10 papers

on Plastid genes

Issue of 2019‒03‒10
seven papers selected by
Vera S. Bogdanova
Institute of Cytology and Genetics, Siberian Branch of the Russian Academy of Sciences

Chloroplast competition is controlled by lipid biosynthesis in evening primroses.
The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast psbJ RNA.
The zinc-finger transcription factor CcLOL1 controls chloroplast development and immature pepper fruit color in Capsicum chinense and its function is conserved in tomato.
Hybridization rate and hybrid fitness for Camelina microcarpa Andrz. ex DC (♀) and Camelina sativa (L.) Crantz(Brassicaceae) (♂).
The interaction between genotype and maternal nutritional environments affects tomato seed and seedling quality.
Reconstruction of Ancestral Genome Reveals Chromosome Evolution History for Selected Legume Species.
Fitness costs associated with acetyl-coenzyme A carboxylase mutations endowing herbicide resistance in American sloughgrass (Beckmannia syzigachne Steud.).

Proc Natl Acad Sci U S A. 2019 Mar 04. pii: 201811661. [Epub ahead of print]

Chloroplast competition is controlled by lipid biosynthesis in evening primroses.

Johanna Sobanski, Patrick Giavalisco, Axel Fischer, Julia M Kreiner, Dirk Walther, Mark Aurel Schöttler, Tommaso Pellizzer, Hieronim Golczyk, Toshihiro Obata, Ralph Bock, Barbara B Sears, Stephan Greiner.

  In most eukaryotes, organellar genomes are transmitted preferentially by the mother, but molecular mechanisms and evolutionary forces underlying this fundamental biological principle are far from understood. It is believed that biparental inheritance promotes competition between the cytoplasmic organelles and allows the spread of so-called selfish cytoplasmic elements. Those can be, for example, fast-replicating or aggressive chloroplasts (plastids) that are incompatible with the hybrid nuclear genome and therefore maladaptive. Here we show that the ability of plastids to compete against each other is a metabolic phenotype determined by extremely rapidly evolving genes in the plastid genome of the evening primrose Oenothera Repeats in the regulatory region of accD (the plastid-encoded subunit of the acetyl-CoA carboxylase, which catalyzes the first and rate-limiting step of lipid biosynthesis), as well as in ycf2 (a giant reading frame of still unknown function), are responsible for the differences in competitive behavior of plastid genotypes. Polymorphisms in these genes influence lipid synthesis and most likely profiles of the plastid envelope membrane. These in turn determine plastid division and/or turnover rates and hence competitiveness. This work uncovers cytoplasmic drive loci controlling the outcome of biparental chloroplast transmission. Here, they define the mode of chloroplast inheritance, as plastid competitiveness can result in uniparental inheritance (through elimination of the "weak" plastid) or biparental inheritance (when two similarly "strong" plastids are transmitted).

Keywords:  acetyl-CoA carboxylase; biparental inheritance; correlation mapping; selfish cytoplasmic elements; ycf2

DOI:  https://doi.org/10.1073/pnas.1811661116
Plant J. 2019 Mar 07.

The Arabidopsis pentatricopeptide repeat protein LPE1 and its maize ortholog are required for translation of the chloroplast psbJ RNA.

Rosalind Williams-Carrier, Carolyn Brewster, Susan E Belcher, Margarita Rojas, Prakitchai Chotewutmontri, Sonja Ljungdahl, Alice Barkan.

  The expression of chloroplast genes relies on a host of nucleus-encoded proteins. Identification of such proteins and elucidation of their functions are ongoing challenges. We used ribosome profiling to revisit the function of the pentatricopeptide repeat protein LPE1, reported to stimulate translation of the chloroplast psbA mRNA in Arabidopsis. Mutation of the maize LPE1 ortholog causes a photosystem II (PSII) deficiency and a defect in translation of the chloroplast psbJ open reading frame (ORF) but has no effect on psbA expression. To reflect this function, we named the maize LPE1 ortholog Translation of psbJ 1 (TPJ1). Arabidopsis lpe1 mutants likewise exhibit a loss of psbJ translation, and have, in addition, a decrease in psbN translation. We detected a small decrease in ribosome occupancy on the psbA mRNA in Arabidopsis lpe1 mutants, but ribosome profiling analyses of other PSII mutants (hcf107 and hcf173) in conjunction with in vitro RNA binding data strongly suggest that this is a secondary effect of their PSII deficiency. We conclude that maize TPJ1 promotes PSII synthesis by activating translation of the psbJ ORF, that this function is conserved in Arabidopsis LPE1, and that an additional role for LPE1 in psbN translation contributes to the PSII deficiency in lpe1 mutants. This article is protected by copyright. All rights reserved.

Keywords:   PPR ; Arabidopsis; chloroplast; hcf107; hcf173; lpe1; maize; plastid; psbA; psbJ; psbN

DOI:  https://doi.org/10.1111/tpj.14308
Plant J. 2019 Mar 03.

The zinc-finger transcription factor CcLOL1 controls chloroplast development and immature pepper fruit color in Capsicum chinense and its function is conserved in tomato.

Yelena Borovsky, Noam Monsonego, Vijee Mohan, Sara Shabtai, Itzhak Kamara, Adi Faigenboim, Theresa Hill, Shiyu Chen, Kevin Stoffel, Allen Van Deynze, Ilan Paran.

  Chloroplast development and chlorophyll content in the immature fruit has a major impact on the morphology and quality in pepper (Capsicum spp.) fruit. Two major QTLs, pc1 and pc10, that affect chlorophyll content in the pepper fruit by modulation of chloroplast compartment size were previously identified in chromosomes 1 and 10, respectively. The pepper homolog of GOLDEN2-LIKE transcription factor (CaGLK2) has been found as underlying pc10, similar to its effect on tomato chloroplast development. In the present study, we identified the pepper homolog of the zinc-finger transcription factor LOL1 (LSD ONE LIKE1; CcLOL1) as the gene underlying pc1. LOL1 has been identified in Arabidopsis as a positive regulator of programmed cell death and we report here on its role in controlling fruit development in the Solanaceae in a fruit-specific manner. The light-green C. chinense parent used for QTL mapping was found to carry a null mutation in CcLOL1. Verification of the function of the gene was done by generating CRISPR/Cas9 knockout mutants of the orthologous tomato gene resulting in light-green tomato fruits, indicating functional conservation of the orthologous genes in controlling chlorophyll content in the Solanaceae. Transcriptome profiling of light and dark-green bulks differing for pc1, showed that the QTL affects multiple photosynthesis and oxidation-reduction associated genes in the immature green fruit. Allelic diversity of three known genes CcLOL1, CaGLK2 and CcAPRR2 that influence pepper immature fruit color, was found to be associated with variation in chlorophyll content primarily in C. chinense. This article is protected by copyright. All rights reserved.

Keywords:  Chloroplast development; chlorophyll content; fruit development; pepper (Capsicum spp.); tomato (Solanum lycopersicum); zinc-finger transcription factor

DOI:  https://doi.org/10.1111/tpj.14305
Evol Appl. 2019 Mar;12(3): 443-455

Hybridization rate and hybrid fitness for Camelina microcarpa Andrz. ex DC (♀) and Camelina sativa (L.) Crantz(Brassicaceae) (♂).

Sara L Martin, Beatriz E Lujan-Toro, Connie A Sauder, Tracey James, Sara Ohadi, Linda M Hall.

  Hybridization between crops and their wild relatives has the potential to introduce novel variation into wild populations. Camelina (Camelina sativa) is a promising oilseed and cultivars with modified seed characteristics and herbicide resistance are in development, prompting a need to evaluate the potential for novel trait introgression into weedy relatives. Little-podded false flax (littlepod; Camelina microcarpa) is a naturalized weed in Canada and the USA. Here we evaluated the hybridization rate between the three cytotypes of littlepod (♀) and camelina (♂), assessed characteristics of hybrids, and evaluated the fitness of hexaploid littlepod and camelina hybrids in the glasshouse and field. In total we conducted, 1,005 manual crosses with diploid littlepod, 1, 172 crosses with tetraploid littlepod, and 896 crosses with hexaploid littlepod. Hybrids were not produced by the diploids, but were produced by the tetraploids and hexaploids at rates of one hybrid for 2,000 ovules pollinated and 24 hybrids for 25 ovules pollinated, respectively. Hybrids between tetraploid littlepod and camelina showed low pollen fertility and produced a small number of seeds. In the glasshouse, hybrids between hexaploid littlepod and camelina also showed significantly lower pollen fertility and seed production than parental lines, but their seeds showed high viability. A similar pattern was observed in field trials, with hybrids showing earlier flowering, reduced biomass, seed production and seed weight. However, seed produced by the hybrids showed greater viability than that produced by hexaploid littlepod and is potentially the result of a shortened lifecycle. The introgression of lifecycle traits into littlepod populations may facilitate range expansion and contribute to crop gene persistence. Consequently, future work should evaluate the hybridization rate in the field, the fitness of advanced generation backcrosses, and the role of time to maturity in limiting hexaploid littlepod's distribution.

Keywords:  biosafety; crop‐wild hybridization; gene flow; hybrid fitness; inter‐species hybridization

DOI:  https://doi.org/10.1111/eva.12724
J Exp Bot. 2019 Mar 02. pii: erz101. [Epub ahead of print]

The interaction between genotype and maternal nutritional environments affects tomato seed and seedling quality.

Nafiseh Geshnizjani, Saadat Sarikhani Khorami, Leo A J Willems, Basten L Snoek, Henk W M Hilhorst, Wilco Ligterink.

  Seed and seedling traits are affected by the conditions of the maternal environment, such as light, temperature and nutrient availability. In this study, we have investigated whether different maternally applied nitrate and phosphate concentrations affect the seed and seedling performance of two closely related tomato species: Solanum lycopersicum cv. Money maker and Solanum pimpinellifolium accession CGN14498. We observed large differences for seed and seedling traits between the two species. Additionally, we have shown that for nitrate most of the seed and seedling traits were significantly affected by genotype by environment interactions (G×E). The effect of the maternal environment was clearly visible in the primary metabolites of the dry seeds. For example, we could show that the amount of -aminobutyric acid (GABA) in Money maker seeds was affected by the differences in the maternal environments and was positively correlated with seed germination under high temperature. Overall, compared to phosphate, nitrate had a larger effect on seed and seedling performance in tomato. In general, the different responses to the maternal environments of the two tomato species show a major role of genotype by environment interactions in shaping seed and seedling traits.

Keywords:   Solanum lycopersicum ; Solanum pimpinellifolium ; Genotype by environment interaction (G×E); maternal environment; metabolites; seed quality; seedling quality

DOI:  https://doi.org/10.1093/jxb/erz101
New Phytol. 2019 Mar 04.

Reconstruction of Ancestral Genome Reveals Chromosome Evolution History for Selected Legume Species.

Longhui Ren, Wei Huang, Steven B Cannon.

  Reconstruction of an ancestral genome for a set of plant species has been a challenging task because of complex histories that may include whole genome duplications (WGDs), segmental duplications, independent gene duplications or losses, diploidization, and rearrangement events. Here, we describe the reconstruction a hypothetical ancestral genome for the papilionoid legumes (the largest subfamily within the third largest family in flowering plants), and evaluate the results relative to phylogenetic and chromosomal count data for this group of legumes, spanning 294 diverse papilionoid genera. To reconstruct the ancestral genomes for nine legume species with sequenced genomes, we used a maximum likelihood approach combined with a novel method for identifying informative markers for this purpose. Analyzing genomes from four species within the Phaseoleae, two in Dalbergieae, two in the "inverted-repeat-loss" (IRL) clade, and one in the Robinieae, we infer a common ancestral genome with 9 chromosomes. The reconstructed genome structural histories are consistent with chromosomal and phylogenetic histories, but we also infer that a common ancestor with 9 chromosomes was probably intermediate to an earlier state of 14 chromosomes following a whole-genome duplication that predated the radiation of the papilionoid legumes, evidence for which is found in early-diverging papilionoid lineages. This article is protected by copyright. All rights reserved.

Keywords:  Ancestral genome reconstruction; Chromosome evolution history; Maximum Likelihood for Gene-Order (MLGO); Papilionoid legumes; Phylogenetic reconstruction; Syntenic-block marker

DOI:  https://doi.org/10.1111/nph.15770
Ecol Evol. 2019 Feb;9(4): 2220-2230

Fitness costs associated with acetyl-coenzyme A carboxylase mutations endowing herbicide resistance in American sloughgrass (Beckmannia syzigachne Steud.).

Long Du, Mingjing Qu, Xiaojing Jiang, Xiao Li, Qian Ju, Xingtao Lu, Jinxin Wang.

  Weed resistance to herbicide can be conferred by gene mutations, and some mutations can cause pleiotropic effects in some cases. We investigated the pleiotropic effects associated with five specific ACCase mutations (Ile1781Leu, Trp2027Cys, Ile2041Asn, Asp2078Gly, and Gly2096Ala) on the plant growth, seed production, and resource competitiveness in American sloughgrass.Resistant plants (M/M) homozygous for specific ACCase mutation and susceptible wild-type plants (W/W) were derived from single heterozygous mother plant (M/W) by genotyping. Plant growth assay and neighborhood experiments were performed to quantify variation between M/M plants and W/W plants.The Ile1781Leu mutation resulted in slight increases in plant growth in pure stands and improved resource competitiveness under low-competition conditions in pot experiments, but no clear variation was observed under high competitive pressure or field conditions. During competition with wheat plants under field conditions, American sloughgrass plants containing Ile2041Asn ACCase exhibited a significantly lower (12.5%) aboveground biomass but no distinct differences in seed production or resource competitiveness. No significant detrimental pleiotropic effects associated with Gly2096Ala were detected in American sloughgrass.The Trp2027Cys mutation distinctly reduced seed production, especially under high competitive pressure, but did not significantly alter plant growth. The Asp2078Gly mutation consistently reduced not only plant growth and seed production but also resource competitiveness. Synthesis. The Trp2027Cys and Asp2078Gly mutations led to significant fitness costs, which may reduce the frequency of resistance alleles and reduce the propagation speed of resistant weeds in the absence of ACCase inhibitor herbicides. The Ile1781Leu, Ile2041Asn, and Gly2096Ala mutations displayed no obvious fitness costs or displayed very small fitness penalties, which would likely have no effect on the establishment of resistant weeds in the field.

Keywords:  ACCase mutation; competition; evolution of resistance; fitness cost; plant growth; resistance

DOI:  https://doi.org/10.1002/ece3.4917