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Fernie, A. R.

Publications and source records attributed to Fernie, A. R..

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Photoperiod shapes aluminium tolerance in plants

Aluminium is a limiting factor for crop productivity in acidic soils (pH [≤] 5.5). Since acid soil distribution on Earth cannot adequately explain the differential Al tolerance across the plant kingdom, we investigated photoperiod effects on plant Al tolerance. We observed that with increasing distance from the equator, Al tolerance disappears, suggesting a relationship with the photoperiod. Long-day (LD) species are generally more Al-sensitive than short-day (SD) species, whereas genetic conversion of tomato for SD growth boosts Al tolerance. Reduced Al tolerance correlates with DNA-checkpoint activation under LD. DNA-checkpoint-related genes are under positive selection in Arabidopsis accessions from regions with shorter days, suggesting photoperiod acts as a selective barrier for Al tolerance. Our findings revealed that diel regulation and genetic diversity affect Al tolerance, suggesting that day-length orchestrates Al tolerance. One-Sentence SummaryAluminum is a major constraint for crop yield worldwide. We reveal that photoperiod acts as a barrier for Al tolerance in plants.

plant biology↗

Coordinating the morphogenesis-differentiation balance by tweaking the cytokinin-gibberellin equilibrium

Morphogenesis and differentiation are important stages in organ development and shape determination. However, how they are balanced and tuned during development is not fully understood. In the compound leaved tomato, an extended morphogenesis phase allows for the initiation of leaflets, resulting in the compound form. Maintaining a prolonged morphogenetic phase in early stages of compound-leaf development is dependent on delayed activity of several factors that promote differentiation, including CIN-TCP transcription factor (TF) LA, the MYB TF CLAU and the plant hormone Gibberellin (GA). Here, we investigated the genetic regulation of the morphogenesis-differentiation balance by studying the relationship between LA, CLAU and GA. Our genetic and molecular examination suggest that LA is expressed more broadly than CLAU and determines the spatio-temporal context of CLAU activity. We demonstrate that both LA and CLAU affect the Cytokinin/Gibberellin (CK/GA) balance. LA reduces the sensitivity of the leaf margin to CK, shown before to be also affected by CLAU. CLAU affects leaf active GA content and sensitivity, shown previously to be also influenced by LA. Therefore, LA and CLAU likely function in parallel pathways to promote leaf differentiation by converging on common downstream processes, including the CK/GA balance.

plant biology↗

Mild reductions in guard cell sucrose synthase 2 expression leads to slower stomatal opening and decreased whole plant transpiration in tobacco

The understanding of the dynamics of stomatal movements has increased substantially through genetic manipulation of plant metabolism either at the whole plant level or specifically in guard cells. However, the regulation of stomatal speediness remains not completely elucidated. Here we shown that reduced expression of guard cell sucrose synthase 2 (NtSUS2) of Nicotiana tabacum L. altered the topology and the connectivity of the guard cell metabolic network and the accumulation of metabolites positively correlated with stomatal speediness during dark-to-light transition. This leads to a slower light-induced stomatal opening, lower steady-state stomatal conductance and a strong reduction (up to 44%) in daily whole plant transpiration in the transgenics, when compared to wild type plants. Furthermore, the transgenic lines transpired more or have lower reduction in whole plant transpiration under short water deficit periods, indicating a higher effective use of water under this condition. Our results collectively suggest that the regulation of stomatal movement and speediness involve a complex modulation of the guard cell metabolic network, in which NtSUS2 has an important role. The results are discussed on the role of guard cell metabolism for the regulation of both stomatal speediness and whole plant transpiration.

plant biology↗

Hello darkness, my old friend: 3-Ketoacyl-Coenzyme A Synthase4 is a branch point in the regulation of triacylglycerol synthesis in Arabidopsis by re-channeling fatty acids under carbon starvation

Due to their sessile lifestyle, plants have evolved unique mechanisms to deal with environmental challenges. Under stress, plant lipids are important as alternative sources of carbon and energy when sugars or starch are limited. Here, we applied combined heat and darkness and extended darkness to a panel of [~] 300 Arabidopsis accessions to study lipid remodeling under carbon starvation. Natural allelic variation at 3-KETOACYL-COENZYME A SYNTHASE4 (KCS4), a gene encoding for an enzyme involved in very long chain fatty-acid (VLCFA) synthesis, underlies a differential accumulation of polyunsaturated triacylglycerols (puTAGs) under stress. Ectopic expression in yeast and plants proved that KCS4 is a functional enzyme localized in the ER with specificity for C22 and C24 saturated acyl-CoA. Allelic mutants and transient overexpression in planta revealed the differential role of KCS4 alleles in VLCFA synthesis and wax coverage, puTAG accumulation and biomass. Moreover, the region harboring KCS4 is under high selective pressure and allelic variation at KCS4 correlated with environmental parameters from the locales of Arabidopsis accessions. Our results provide evidence that KCS4 plays a decisive role in the subsequent fate of fatty acids released from chloroplast-membrane lipids under carbon starvation. This work sheds light on both plant response mechanisms and the evolutionary events shaping the lipidome under carbon starvation. One sentence summaryNatural variation at KCS4 underlies a differential accumulation of polyunsaturated triacylglycerols under carbon starvation, by acting as a regulatory branch point in the fate of fatty acids.

genetics↗

Kingdom-wide analysis of the evolution of the plant type III polyketide synthase superfamily

The emergence of type III polyketide synthases (PKSs) was a pre-requisite for the conquest of land by the green lineage. To study the deep evolutionary history of this key family, we used phylogenomic synteny network and phylogenetic analyses of whole-genome data from 126 species spanning the green lineage. This study thereby combined study of genomic location and context with changes in gene sequences. We found that two major clades, CHS and LAP5/6 homologs, evolved early by a segmental duplication event prior to the divergence of Bryophytes and Tracheophytes. We propose that the macroevolution of the type III PKS superfamily is governed by whole-genome duplications and triplications. Intriguingly, the combined phylogenetic and synteny analyses in this study shed new insights into changes in the genomic location and context that are retained for a longer time scale with more recent functional divergence captured by gene sequence alterations.

plant biology↗

A Solanum lycopersicoides reference genome facilitates biological discovery in tomato

Wild relatives of tomato are a valuable source of natural variation in tomato breeding, as many can be hybridized to the cultivated species (Solanum lycopersicum). Several, including Solanum lycopersicoides, have been crossed to S. lycopersicum for the development of ordered introgression lines (ILs). Despite the utility of these wild relatives and their associated ILs, limited finished genomes have been produced to aid genetic and genomic studies. We have generated a chromosome-scale genome assembly for Solanum lycopersicoides LA2951 using PacBio sequencing, Illumina, and Hi-C. We identified 37,938 genes based on Illumina and Isoseq and compared gene function to the available cultivated tomato genome resources, in addition to mapping the boundaries of the S. lycopersicoides introgressions in a set of cv. VF36 x LA2951 introgression lines (IL). The genome sequence and IL map will support the development of S. lycopersicoides as a model for studying fruit nutrient/quality, pathogen resistance, and environmental stress tolerance traits that we have identified in the IL population and are known to exist in S. lycopersicoides.

genomics↗

Pod indehiscence in common bean is associated to the fine regulation of PvMYB26 and a non-functional abscission layer

In legumes, pod shattering occurs when mature pods dehisce along the sutures, and detachment of the valves promotes seed dispersal. In Phaseolus vulgaris, the major locus qPD5.1-Pv for pod indehiscence was identified recently. We developed a BC4/F4 introgression line population and narrowed the major locus down to a 22.5-kb region. Here, gene expression and a parallel histological analysis of dehiscent and indehiscent pods identified an AtMYB26 orthologue as the best candidate for loss of pod shattering, on a genomic region ~11 kb downstream of the highest associated peak. Based on mapping and expression data, we propose early and fine up-regulation of PvMYB26 in dehiscent pods. Detailed histological analysis establishes that pod indehiscence is associated to the lack of a functional abscission layer in the ventral sheath, and that the key anatomical modifications associated with pod shattering in common bean occur early during pod development. We finally propose that loss of pod shattering in legumes resulted from histological convergent evolution and that this is the result of selection at orthologous loci. One-sentence summaryA non-functional abscission layer determines the loss of pod shattering; mapping data, and parallel gene expression and histological analysis support PvMYB26 as the candidate gene for pod indehiscence.

genetics↗

qKW9 encodes a pentatricopeptide repeat protein affecting photosynthesis and grain filling in maize

Kernel weight is an important yield component in maize that was selected during domestication. Many kernel weight genes have been identified through mutant analysis, and are mostly involved in the biogenesis and functional maintenance of organelles or other fundamental cellular activities. However, only a limited number of loci underlying quantitative variation in kernel weight have been cloned. Here we characterize a maize kernel weight QTL, qKW9 and find that it encodes a DYW motif pentatricopeptide repeat protein involved in C-to-U editing of NdhB, a subunit of the chloroplast NADH dehydrogenase-like complex. In a null qKW9 background, C-to-U editing of NdhB was abolished, and photosynthesis was reduced, suggesting that qKW9 regulates kernel weight by controling the maternal source of photosynthate for grain filling. Characterization of qKW9 highlights the importance of optimizing photosynthesis on maize grain yield production.

plant biology↗

The Genome of the Charophyte Alga Penium margaritaceum Bears Footprints of the Evolutionary Origins of Land Plants

The colonization of land by plants was a pivotal event in the history of the biosphere, and yet the underlying evolutionary features and innovations of the first land plant ancestors are not well understood. Here we present the genome sequence of the unicellular alga Penium margaritaceum, a member of the Zygnematophyceae, the sister lineage to land plants. The P. margaritaceum genome has a high proportion of repeat sequences, which are associated with massive segmental gene duplications, likely facilitating neofunctionalization. Compared with earlier diverging plant lineages, P. margaritaceum has uniquely expanded repertoires of gene families, signaling networks and adaptive responses, supporting its phylogenetic placement and highlighting the evolutionary trajectory towards terrestrialization. These encompass a broad range of physiological processes and cellular structures, such as large families of extracellular polymer biosynthetic and modifying enzymes involved in cell wall assembly and remodeling. Transcriptome profiling of cells exposed to conditions that are common in terrestrial habitats, namely high light and desiccation, further elucidated key adaptations to the semi-aquatic ecosystems that are home to the Zygnematophyceae. Such habitats, in which a simpler body plan would be advantageous, likely provided the evolutionary crucible in which selective pressures shaped the transition to land. Earlier diverging charophyte lineages that are characterized by more complex land plant-like anatomies have either remained exclusively aquatic, or developed alternative life styles that allow periods of desiccation.

plant biology↗

Phytochrome light receptors control metabolic flux, and their action during seedling development sets the trajectory for biomass production

The phytochromes (phys) photoreceptors are known to be major regulators of plastic growth responses to vegetation shade. Recent reports have begun to uncover an important role for phys in carbon resource management. Our earlier work showed that phy mutants had a distinct metabolic profile with elevated levels of metabolites including TCA intermediates, amino acids and sugars. Here we show that in seedlings phy regulates the balance between glucose and starch. Multi-allele phy mutants have excess glucose and low starch levels, which is conducive to hypocotyl elongation. 13C-CO2 labelling demonstrates that metabolic flux balance in adult plants is markedly altered in phy mutants. Phytochrome reduces synthesis rates of stress metabolites, including raffinose and proline and several typical stress-induced biosynthetic genes related to these metabolites show higher expression in phy mutants.\n\nSince growth and metabolism are typically inter-connected, we investigated why phy mutants have severely reduced biomass. Quantification of carbon fixation, biomass accumulation, and 13C labelling of cell wall polysaccharides established that relative growth rate is impaired in multi allele phy mutants for the first 2.5 weeks after germination but equivalent to the WT thereafter. Mathematical modelling predicts that the altered growth dynamics and final biomass deficit can be explained by the smaller cotyledon size of the multiple phy mutants. This indicates that the established role of phy in promoting seedling establishment has enduring effects that govern adult plant biomass.

plant biology↗

Expression atlas of Selaginella moellendorffii provides insights into the evolution of vasculature, secondary metabolism and roots

O_LIThe lycophyte Selaginella moellendorffii represents early vascular plants and is studied to understand the evolution of higher plant traits such as the vasculature, leaves, stems, roots, and secondary metabolism. However, little is known about the gene expression and transcriptional coordination of Selaginella genes, which precludes us from understanding the evolution of transcriptional programs behind these traits.\nC_LIO_LIWe here present a gene expression atlas comprising all major organs, tissue types, and the diurnal gene expression profiles for S. moellendorffii. The atlas is part of the CoNekT-Plants database (conekt.plant.tools), which enables comparative transcriptomic analyses across two algae and seven land plants.\nC_LIO_LIWe show that the transcriptional gene module responsible for the biosynthesis of lignocellulose evolved in the ancestor of vascular plants, and pinpoint the duplication and subfunctionalization events that generated multiple gene modules involved in the biosynthesis of various cell wall types. We further demonstrate how secondary metabolism is transcriptionally coordinated and integrated with other cellular pathways. Finally, we identify root-specific genes in vascular plants and show that the evolution of roots did not coincide with an increased appearance of gene families, suggesting that the existing genetic material was sufficient to generate new organs.\nC_LIO_LIOur updated database at conekt.plant.tools provides a unique resource to study the evolution of genes, gene families, transcriptomes, and functional gene modules in the Archaeplastida kingdom.\nC_LI

plant biology↗

Increased expression of mitochondrial dysfunction stimulon genes affects chloroplast redox status and photosynthetic electron transfer in Arabidopsis

Mitochondrial retrograde signals control expression of nuclear mitochondrial dysfunction stimulon (MDS) genes. Although MDS gene products mostly affect mitochondrial functions, they also influence production of reactive oxygen species (ROS) and redox status of chloroplasts. To study this inter-organellar interaction, we analysed the response of the Arabidopsis MDS-overexpressor mutant rcd1 to methyl viologen (MV), which catalyses electron transfer from Photosystem I (PSI) to molecular oxygen, generating ROS in Mehlers reaction. The response of plants to MV was investigated by imaging chlorophyll fluorescence in aerobic and hypoxic environments, and by membrane inlet mass spectrometry. Hypoxic treatment abolished the effect of MV on photosynthetic electron transfer in rcd1, but not in wild type. A similar reaction to hypoxia was observed in other MDS-activating lines and treatments. This suggests that MDS gene products contribute to oxygen depletion at the PSI electron-acceptor side. In unstressed growth conditions this MDS-related effect is likely masked by endogenous oxygen evolution and gas exchange with the atmosphere. In rcd1, altered Mehlers reaction coincided with more reduced state of the chloroplast NADPH-thioredoxin oxidoreductase C (NTRC) and its targets, suggesting that NTRC performs feedback control of photosynthesis. This regulation may represent a novel mechanism whereby mitochondrial retrograde signalling affects chloroplast functions.

plant biology↗

The genome and metabolome of the tobacco tree, Nicotiana glauca: a potential renewable feedstock for the bioeconomy

BackgroundGiven its tolerance to stress and its richness in particular secondary metabolites, the tobacco tree, Nicotiana glauca, has been considered a promising biorefinery feedstock that would not be competitive with food and fodder crops.\n\nResultsHere we present a 3.5 Gbp draft sequence and annotation of the genome of N. glauca spanning 731,465 scaffold sequences, with an N50 size of approximately 92 kbases. Furthermore, we supply a comprehensive transcriptome and metabolome analysis of leaf development comprising multiple techniques and platforms.\n\nThe genome sequence is predicted to cover nearly 80% of the estimated total genome size of N. glauca. With 73,799 genes predicted and a BUSCO score of 94.9%, we have assembled the majority of gene-rich regions successfully. RNA-Seq data revealed stage-and/or tissue-specific expression of genes, and we determined a general trend of a decrease of tricarboxylic acid cycle metabolites and an increase of terpenoids as well as some of their corresponding transcripts during leaf development.\n\nConclusionThe N. glauca draft genome and its detailed transcriptome, together with paired metabolite data, constitute a resource for future studies of valuable compound analysis in tobacco species and present the first steps towards a further resolution of phylogenetic, whole genome studies in tobacco.

plant biology↗

RCD1 Coordinates Chloroplastic and Mitochondrial Electron Transfer through Interaction with ANAC Transcription Factors

Signaling from chloroplasts and mitochondria, both dependent on reactive oxygen species (ROS), merge at the nuclear protein RADICAL-INDUCED CELL DEATH1 (RCD1). ROS produced in the chloroplasts affect the abundance, thiol redox state and oligomerization of RCD1. RCD1 directly interacts in vivo with ANAC013 and ANAC017 transcription factors, which are the mediators of the ROS-related mitochondrial complex III retrograde signa and suppresses activity of ANAC013 and ANAC017. Inactivation of RCD1 leads to increased expression of ANAC013 and ANAC017-regulated genes belonging to the mitochondrial dysfunction stimulon (MDS), including genes for mitochondrial alternative oxidases (AOXs). Accumulating AOXs and other MDS gene products alter electron transfer pathways in the chloroplasts, leading to diminished production of chloroplastic ROS and increased protection of photosynthetic apparatus from ROS damage. RCD1-dependent regulation affects chloroplastic and mitochondrial retrograde signaling including chloroplast signaling by 3-phosphoadenosine 5-phosphate (PAP). Sensitivity of RCD1 to organellar ROS provides feedback control of nuclear gene expression.

plant biology↗

Reconstructing The Gigabase Plant Genome Of Solanum pennellii Using Nanopore Sequencing

Recent updates in sequencing technology have made it possible to obtain Gigabases of sequence data from one single flowcell. Prior to this update, the nanopore sequencing technology was mainly used to analyze and assemble microbial samples1-3. Here, we describe the generation of a comprehensive nanopore sequencing dataset with a median fragment size of 11,979 bp for the wild tomato species Solanum pennellii featuring an estimated genome size of ca 1.0 to 1.1 Gbases. We describe its genome assembly to a contig N50 of 2.5 MB using a pipeline comprising a Canu4 pre-processing and a subsequent assembly using SMARTdenovo. We show that the obtained nanopore based de novo genome reconstruction is structurally highly similar to that of the reference S. pennellii LA7165 genome but has a high error rate caused mostly by deletions in homopolymers. After polishing the assembly with Illumina short read data we obtained an error rate of <0.02 % when assessed versus the same Illumina data. More importantly however we obtained a gene completeness of 96.53% which even slightly surpasses that of the reference S. pennellii genome5. Taken together our data indicate such long read sequencing data can be used to affordably sequence and assemble Gbase sized diploid plant genomes.\n\nRaw data is available at http://www.plabipd.de/portal/solanum-pennellii and has been deposited as PRJEB19787.

genomics↗