Publications by authors named "Jeffrey L Bennetzen"

130 Publications

Integration of high-density genetic mapping with transcriptome analysis uncovers numerous agronomic QTL and reveals candidate genes for the control of tillering in sorghum.

G3 (Bethesda) 2021 Feb;11(2)

Department of Biology, West Virginia University, Morgantown, WV 26505, USA.

Phenotypes such as branching, photoperiod sensitivity, and height were modified during plant domestication and crop improvement. Here, we perform quantitative trait locus (QTL) mapping of these and other agronomic traits in a recombinant inbred line (RIL) population derived from an interspecific cross between Sorghum propinquum and Sorghum bicolor inbred Tx7000. Using low-coverage Illumina sequencing and a bin-mapping approach, we generated ∼1920 bin markers spanning ∼875 cM. Phenotyping data were collected and analyzed from two field locations and one greenhouse experiment for six agronomic traits, thereby identifying a total of 30 QTL. Many of these QTL were penetrant across environments and co-mapped with major QTL identified in other studies. Other QTL uncovered new genomic regions associated with these traits, and some of these were environment-specific in their action. To further dissect the genetic underpinnings of tillering, we complemented QTL analysis with transcriptomics, identifying 6189 genes that were differentially expressed during tiller bud elongation. We identified genes such as Dormancy Associated Protein 1 (DRM1) in addition to various transcription factors that are differentially expressed in comparisons of dormant to elongating tiller buds and lie within tillering QTL, suggesting that these genes are key regulators of tiller elongation in sorghum. Our study demonstrates the usefulness of this RIL population in detecting domestication and improvement-associated genes in sorghum, thus providing a valuable resource for genetic investigation and improvement to the sorghum community.
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http://dx.doi.org/10.1093/g3journal/jkab024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8022972PMC
February 2021

Genome sequence and genetic diversity analysis of an under-domesticated orphan crop, white fonio (Digitaria exilis).

Gigascience 2021 03;10(3)

Department of Plant Sciences, Seed Biotechnology Center, University of California, 1 Shields Ave. Davis, CA 95616, USA.

Background: Digitaria exilis, white fonio, is a minor but vital crop of West Africa that is valued for its resilience in hot, dry, and low-fertility environments and for the exceptional quality of its grain for human nutrition. Its success is hindered, however, by a low degree of plant breeding and improvement.

Findings: We sequenced the fonio genome with long-read SMRT-cell technology, yielding a ∼761 Mb assembly in 3,329 contigs (N50, 1.73 Mb; L50, 126). The assembly approaches a high level of completion, with a BUSCO score of >99%. The fonio genome was found to be a tetraploid, with most of the genome retained as homoeologous duplications that differ overall by ∼4.3%, neglecting indels. The 2 genomes within fonio were found to have begun their independent divergence ∼3.1 million years ago. The repeat content (>49%) is fairly standard for a grass genome of this size, but the ratio of Gypsy to Copia long terminal repeat retrotransposons (∼6.7) was found to be exceptionally high. Several genes related to future improvement of the crop were identified including shattering, plant height, and grain size. Analysis of fonio population genetics, primarily in Mali, indicated that the crop has extensive genetic diversity that is largely partitioned across a north-south gradient coinciding with the Sahel and Sudan grassland domains.

Conclusions: We provide a high-quality assembly, annotation, and diversity analysis for a vital African crop. The availability of this information should empower future research into further domestication and improvement of fonio.
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http://dx.doi.org/10.1093/gigascience/giab013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7953496PMC
March 2021

Discovery and characterization of tannase genes in plants: roles in hydrolysis of tannins.

New Phytol 2020 05 15;226(4):1104-1116. Epub 2020 Feb 15.

State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, 230036, Hefei, China.

Plant tannins, including condensed tannins (CTs) and hydrolyzable tannins (HTs), are widely distributed in the plant kingdom. To date, tannase (TA) - is a type of tannin acyl-hydrolase hydrolyzing HTs, CT monomer gallates and depsides - has been reported in microbes only. Whether plants express TA remains unknown. Herein, we report plant TA genes. A native Camellia sinensis TA (CsTA) is identified from leaves. Six TAs are cloned from tea, strawberry (Fragaria × ananassa, Fa) and four other crops. Biochemical analysis shows that the native CsTA and six recombinant TAs hydrolyze tannin compounds, depsides and phenolic glycosides. Transcriptional and metabolic analyses reveal that the expression of CsTA is oppositely associated with the accumulation of galloylated catechins. Moreover, the transient overexpression and RNA interference of FaTA are positively associated with the accumulation of ellagitannins in strawberry fruit. Phylogenetic analysis across different kingdoms shows that 29 plant TA homologs are clustered as a plant-specific TA clade in class I carboxylesterases. Further analysis across the angiosperms reveals that these TA genes are dispersed in tannin-rich plants, which share a single phylogenetic origin c. 120 million yr ago. Plant TA is discovered for the first time in the plant kingdom and is shown to be valuable to improve tannin compositions in plants.
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http://dx.doi.org/10.1111/nph.16425DOI Listing
May 2020

Exceptional subgenome stability and functional divergence in the allotetraploid Ethiopian cereal teff.

Nat Commun 2020 02 14;11(1):884. Epub 2020 Feb 14.

J. Craig Venter Institute, La Jolla, CA, 92037, USA.

Teff (Eragrostis tef) is a cornerstone of food security in the Horn of Africa, where it is prized for stress resilience, grain nutrition, and market value. Here, we report a chromosome-scale assembly of allotetraploid teff (variety Dabbi) and patterns of subgenome dynamics. The teff genome contains two complete sets of homoeologous chromosomes, with most genes maintaining as syntenic gene pairs. TE analysis allows us to estimate that the teff polyploidy event occurred ~1.1 million years ago (mya) and that the two subgenomes diverged ~5.0 mya. Despite this divergence, we detect no large-scale structural rearrangements, homoeologous exchanges, or biased gene loss, in contrast to many other allopolyploids. The two teff subgenomes have partitioned their ancestral functions based on divergent expression across a diverse expression atlas. Together, these genomic resources will be useful for accelerating breeding of this underutilized grain crop and for fundamental insights into polyploid genome evolution.
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http://dx.doi.org/10.1038/s41467-020-14724-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7021729PMC
February 2020

5Gs for crop genetic improvement.

Curr Opin Plant Biol 2020 08 28;56:190-196. Epub 2020 Jan 28.

Department of Genetics, University of Georgia, Athens, GA 30602, USA.

Here we propose a 5G breeding approach for bringing much-needed disruptive changes to crop improvement. These 5Gs are Genome assembly, Germplasm characterization, Gene function identification, Genomic breeding (GB), and Gene editing (GE). In our view, it is important to have genome assemblies available for each crop and a deep collection of germplasm characterized at sequencing and agronomic levels for identification of marker-trait associations and superior haplotypes. Systems biology and sequencing-based mapping approaches can be used to identify genes involved in pathways leading to the expression of a trait, thereby providing diagnostic markers for target traits. These genes, markers, haplotypes, and genome-wide sequencing data may be utilized in GB and GE methodologies in combination with a rapid cycle breeding strategy.
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http://dx.doi.org/10.1016/j.pbi.2019.12.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7450269PMC
August 2020

Genome Sequence Analysis of sp. C6, Found in the Pitcher Fluids of .

Microbiol Resour Announc 2020 Jan 16;9(3). Epub 2020 Jan 16.

Institute of Bioinformatics, University of Georgia, Athens, Georgia, USA

An unclassified strain was isolated from the pitcher fluids of a pitcher plant growing at Splinter Hill Bog in Alabama. Its genome was sequenced using the Illumina platform. A genome assembly of 4,673,815 bp was obtained. In total, 4,646 protein-encoding sequences and 72 RNA genes are predicted from this assembly.
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http://dx.doi.org/10.1128/MRA.01214-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6965575PMC
January 2020

phylogeny, and analysis of genetic variation in a diverse collection of date palm () and related species.

Plant Divers 2019 Oct 18;41(5):330-339. Epub 2018 Dec 18.

Department of Genetics, University of Georgia, Athens, GA, USA.

Date palm (), one of the most ancient crops, is grown commercially in >30 countries. Using whole plastome assemblies, phylogenetic analyses revealed that cultivated date palm accessions share the same clade with , and , which are native to the Indian subcontinent, and that is native to the Arabian Peninsula and the deserts of Somalia. Analysis of genetic diversity and genetic relationships among date palm accessions from 13 producing countries involved 195 date palm accessions that were genotyped at 19 microsatellite loci. Extensive genetic diversity was observed, with many accessions heterozygous for most markers in this clonally propagated crop. The average number of alleles per locus (42.1), expected heterozygosity (0.8), observed heterozygosity (0.47) and fixation indices (F = 0.42) demonstrated substantial genetic diversity and population structure. Iraqi accessions were found to have the richest allelic diversity, and the most private alleles. The model-based Bayesian method indicated that these accessions could be broadly divided into two structure groups, one group with predominantly African accessions and another predominantly Asian. Some germplasm, especially from Tunisia and Iraq, deviated from this generalization. Many accessions in the STRUCTURE-derived groups were found to be genetic admixtures, with gene flow between Asian and African groups. Indian and Pakistani date palms were found to be most closely related to North African germplasm.
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http://dx.doi.org/10.1016/j.pld.2018.11.005DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6951277PMC
October 2019

Draft Genome Sequence of a Serratia marcescens Strain Isolated from the Pitcher Fluids of a Pitcher Plant.

Microbiol Resour Announc 2020 Jan 9;9(2). Epub 2020 Jan 9.

Institute of Bioinformatics, University of Georgia, Athens, Georgia, USA

The genome of a strain (C7) that was found in the pitcher fluids of a pitcher plant was sequenced using the Illumina platform. A 5,543,750-bp genome assembly was obtained. A total of 6,278 coding sequences are predicted from this assembly.
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http://dx.doi.org/10.1128/MRA.01216-19DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6952653PMC
January 2020

The bracteatus pineapple genome and domestication of clonally propagated crops.

Nat Genet 2019 10 30;51(10):1549-1558. Epub 2019 Sep 30.

FAFU and UIUC-SIB Joint Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Key Laboratory of Genetics, Breeding and Multiple Utilization of Crops, Ministry of Education, Fujian Agriculture and Forestry University, Fuzhou, China.

Domestication of clonally propagated crops such as pineapple from South America was hypothesized to be a 'one-step operation'. We sequenced the genome of Ananas comosus var. bracteatus CB5 and assembled 513 Mb into 25 chromosomes with 29,412 genes. Comparison of the genomes of CB5, F153 and MD2 elucidated the genomic basis of fiber production, color formation, sugar accumulation and fruit maturation. We also resequenced 89 Ananas genomes. Cultivars 'Smooth Cayenne' and 'Queen' exhibited ancient and recent admixture, while 'Singapore Spanish' supported a one-step operation of domestication. We identified 25 selective sweeps, including a strong sweep containing a pair of tandemly duplicated bromelain inhibitors. Four candidate genes for self-incompatibility were linked in F153, but were not functional in self-compatible CB5. Our findings support the coexistence of sexual recombination and a one-step operation in the domestication of clonally propagated crops. This work guides the exploration of sexual and asexual domestication trajectories in other clonally propagated crops.
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http://dx.doi.org/10.1038/s41588-019-0506-8DOI Listing
October 2019

Comparative transcriptomic analysis reveals gene expression associated with cold adaptation in the tea plant Camellia sinensis.

BMC Genomics 2019 Jul 31;20(1):624. Epub 2019 Jul 31.

State Key Laboratory of Tea Plant Biology and Utilization/International Joint Laboratory on Tea Chemistry and Health Effects, Anhui Agricultural University, West 130 Changjiang Road, Hefei, 230036, Anhui, People's Republic of China.

Background: Low temperature restricts the planting range of all crops, but cold acclimation induces adaption to cold stress in many plants. Camellia sinensis, a perennial evergreen tree that is the source of tea, is mainly grown in warm areas. Camellia sinensis var. sinensis (CSS) has greater cold tolerance than Camellia sinensis var. assamica (CSA). To gain deep insight into the molecular mechanisms underlying cold adaptation, we investigated the physiological responses and transcriptome profiles by RNA-Seq in two tea varieties, cold resistant SCZ (classified as CSS) and cold susceptible YH9 (classified as CSA), during cold acclimation.

Results: Under freezing stress, lower relative electrical conductivity and higher chlorophyll fluorescence (Fv/Fm) values were detected in SCZ than in YH9 when subjected to freezing acclimation. During cold treatment, 6072 and 7749 DEGs were observed for SCZ and YH9, respectively. A total of 978 DEGs were common for both SCZ and YH9 during the entire cold acclimation process. DEGs were enriched in pathways of photosynthesis, hormone signal transduction, and transcriptional regulation of plant-pathogen interactions. Further analyses indicated that decreased expression of Lhca2 and higher expression of SnRK2.8 are correlated with cold tolerance in SCZ.

Conclusions: Compared with CSA, CSS was significantly more resistant to freezing after cold acclimation, and this increased resistance was associated with an earlier expression of cold-induced genes. Because the greater transcriptional differentiation during cold acclimation in SCZ may contribute to its greater cold tolerance, our studies identify specific genes involved in photoinhibition, ABA signal conduction, and plant immunity that should be studied for understanding the processes involved in cold tolerance. Marker-assisted breeding focused on the allelic variation at these loci provides an avenue for the possible generation of CSA cultivars that have CSS-level cold tolerance.
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http://dx.doi.org/10.1186/s12864-019-5988-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6670155PMC
July 2019

The tea plant reference genome and improved gene annotation using long-read and paired-end sequencing data.

Sci Data 2019 07 15;6(1):122. Epub 2019 Jul 15.

State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, 230036, China.

Tea is a globally consumed non-alcohol beverage with great economic importance. However, lack of the reference genome has largely hampered the utilization of precious tea plant genetic resources towards breeding. To address this issue, we previously generated a high-quality reference genome of tea plant using Illumina and PacBio sequencing technology, which produced a total of 2,124 Gb short and 125 Gb long read data, respectively. A hybrid strategy was employed to assemble the tea genome that has been publicly released. We here described the data framework used to generate, annotate and validate the genome assembly. Besides, we re-predicted the protein-coding genes and annotated their putative functions using more comprehensive omics datasets with improved training models. We reassessed the assembly and annotation quality using the latest version of BUSCO. These data can be utilized to develop new methodologies/tools for better assembly of complex genomes, aid in finding of novel genes, variations and evolutionary clues associated with tea quality, thus help to breed new varieties with high yield and better quality in the future.
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http://dx.doi.org/10.1038/s41597-019-0127-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6629666PMC
July 2019

Lateral transfers of large DNA fragments spread functional genes among grasses.

Proc Natl Acad Sci U S A 2019 03 20;116(10):4416-4425. Epub 2019 Feb 20.

Animal and Plant Sciences, University of Sheffield, Western Bank, S10 2TN Sheffield, United Kingdom;

A fundamental tenet of multicellular eukaryotic evolution is that vertical inheritance is paramount, with natural selection acting on genetic variants transferred from parents to offspring. This lineal process means that an organism's adaptive potential can be restricted by its evolutionary history, the amount of standing genetic variation, and its mutation rate. Lateral gene transfer (LGT) theoretically provides a mechanism to bypass many of these limitations, but the evolutionary importance and frequency of this process in multicellular eukaryotes, such as plants, remains debated. We address this issue by assembling a chromosome-level genome for the grass , a species surmised to exhibit two LGTs, and screen it for other grass-to-grass LGTs using genomic data from 146 other grass species. Through stringent phylogenomic analyses, we discovered 57 additional LGTs in the nuclear genome, involving at least nine different donor species. The LGTs are clustered in 23 laterally acquired genomic fragments that are up to 170 kb long and have accumulated during the diversification of The majority of the 59 LGTs in are expressed, and we show that they have added functions to the recipient genome. Functional LGTs were further detected in the genomes of five other grass species, demonstrating that this process is likely widespread in this globally important group of plants. LGT therefore appears to represent a potent evolutionary force capable of spreading functional genes among distantly related grass species.
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http://dx.doi.org/10.1073/pnas.1810031116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6410850PMC
March 2019

Genome sequence of Malania oleifera, a tree with great value for nervonic acid production.

Gigascience 2019 02;8(2)

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, School of Nature Conservation, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China.

Background: Malania oleifera, a member of the Olacaceae family, is an IUCN red listed tree, endemic and restricted to the Karst region of southwest China. This tree's seed is valued for its high content of precious fatty acids (especially nervonic acid). However, studies on its genetic makeup and fatty acid biogenesis are severely hampered by a lack of molecular and genetic tools.

Findings: We generated 51 Gb and 135 Gb of raw DNA sequences, using Pacific Biosciences (PacBio) single-molecule real-time and 10× Genomics sequencing, respectively. A final genome assembly, with a scaffold N50 size of 4.65 Mb and a total length of 1.51 Gb, was obtained by primary assembly based on PacBio long reads plus scaffolding with 10× Genomics reads. Identified repeats constituted ∼82% of the genome, and 24,064 protein-coding genes were predicted with high support. The genome has low heterozygosity and shows no evidence for recent whole genome duplication. Metabolic pathway genes relating to the accumulation of long-chain fatty acid were identified and studied in detail.

Conclusions: Here, we provide the first genome assembly and gene annotation for M. oleifera. The availability of these resources will be of great importance for conservation biology and for the functional genomics of nervonic acid biosynthesis.
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http://dx.doi.org/10.1093/gigascience/giy164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6377399PMC
February 2019

Species-Associated Differences in the Below-Ground Microbiomes of Wild and Domesticated .

Front Plant Sci 2018 21;9:1183. Epub 2018 Aug 21.

Department of Genetics, University of Georgia, Athens, GA, United States.

The rhizosphere microbiome is known to play a crucial role in promoting plant growth, partly by countering soil-borne phytoparasites and by improving nutrient uptake. The abundance and composition of the rhizosphere and root-associated microbiota are influenced by several factors, including plant species and genotype. We hypothesize that crop domestication might influence the composition and diversity of plant-associated microbiomes. We tested the contribution of domestication to the bacterial and archaeal root and soil composition associated with six genotypes of domesticated and four genotypes of its wild ancestor, The bacterial microbiome in the rhizoplane and root endophyte compartments, and the archaea in the endophyte compartment, showed major composition differences. For instance, members of the Betaproteobacteria and Firmicutes were overrepresented in root samples compared to Metagenomic analysis of samples that contained both root surface-bound (rhizoplane) and inside-root (endophytic) bacteria defined two unique microbial communities only associated with roots and one only associated with roots. Root endophytic bacteria were found in six discernible communities, of which four were primarily on and two primarily on . Among archaea, Methanobacteria, and Methanomicrobia exhibited species-associated differences in the rhizosphere and root compartments, but most detected archaea were not classified more specifically than at the level of phylum. These results indicate a host genetic contribution to the microbial composition in , and suggest that domestication has selected for specific associations in the root and in the rhizosphere.
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http://dx.doi.org/10.3389/fpls.2018.01183DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6111228PMC
August 2018

Birth and Death of LTR-Retrotransposons in .

Genetics 2018 11 29;210(3):1039-1051. Epub 2018 Aug 29.

Department of Statistics, University of California, Davis, California 95616.

Long terminal repeat-retrotransposons (LTR-RTs) are a major component of all flowering plant genomes. To analyze the time dynamics of LTR-RTs, we modeled the insertion rates of the 35 most abundant LTR-RT families in the genome of , one of the progenitors of wheat. Our model of insertion rate (birth) takes into account random variation in LTR divergence and the deletion rate (death) of LTR-RTs. Modeling the death rate is crucial because ignoring it would underestimate insertion rates in the distant past. We rejected the hypothesis of constancy of insertion rates for all 35 families and showed by simulations that our hypothesis test controlled the false-positive rate. LTR-RT insertions peaked from 0.064 to 2.39 MYA across the 35 families. Among other effects, the average age of elements within a family was negatively associated with recombination rate along a chromosome, with proximity to the closest gene, and weakly associated with the proximity to its 5' end. Elements within a family that were near genes colinear with genes in the genome of tetraploid emmer wheat tended to be younger than those near noncolinear genes. We discuss these associations in the context of genome evolution and stability of genome sizes in the tribe Triticeae. We demonstrate the general utility of our models by analyzing the two most abundant LTR-RT families in , and show that these families differed in their insertion dynamics. Our estimation methods are available in the R package TE on CRAN.
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http://dx.doi.org/10.1534/genetics.118.301198DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6218219PMC
November 2018

Circular RNA architecture and differentiation during leaf bud to young leaf development in tea (Camellia sinensis).

Planta 2018 Dec 20;248(6):1417-1429. Epub 2018 Aug 20.

State Key Laboratory of Tea Plant Biology and Utilization, Anhui Agricultural University, Hefei, 230036, China.

Main Conclusion: Circular RNA (circRNA) discovery, expression patterns and experimental validation in developing tea leaves indicates its correlation with circRNA-parental genes and potential roles in ceRNA interaction network. Circular RNAs (circRNAs) have recently emerged as a novel class of abundant endogenous stable RNAs produced by circularization with regulatory potential. However, identification of circRNAs in plants, especially in non-model plants with large genomes, is challenging. In this study, we undertook a systematic identification of circRNAs from different stage tissues of tea plant (Camellia sinensis) leaf development using rRNA-depleted circular RNA-seq. By combining two state-of-the-art detecting tools, we characterized 3174 circRNAs, of which 342 were shared by each approach, and thus considered high-confidence circRNAs. A few predicted circRNAs were randomly chosen, and 20 out of 24 were experimental confirmed by PCR and Sanger sequencing. Similar in other plants, tissue-specific expression was also observed for many C. sinensis circRNAs. In addition, we found that circRNA abundances were positively correlated with the mRNA transcript abundances of their parental genes. qRT-PCR validated the differential expression patterns of circRNAs between leaf bud and young leaf, which also indicated the low expression abundance of circRNAs compared to the standard mRNAs from the parental genes. We predicted the circRNA-microRNA interaction networks, and 54 of the differentially expressed circRNAs were found to have potential tea plant miRNA binding sites. The gene sets encoding circRNAs were significantly enriched in chloroplasts related GO terms and photosynthesis/metabolites biosynthesis related KEGG pathways, suggesting the candidate roles of circRNAs in photosynthetic machinery and metabolites biosynthesis during leaf development.
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http://dx.doi.org/10.1007/s00425-018-2983-xDOI Listing
December 2018

Analysis of retrotransposon abundance, diversity and distribution in holocentric Eleocharis (Cyperaceae) genomes.

Ann Bot 2018 08;122(2):279-290

Laboratory of Cytogenetics and Plant Diversity, Department of General Biology, Center for Biological Sciences, State University of Londrina, Londrina, Paraná, Brazil.

Background And Aims: Long terminal repeat-retrotransposons (LTR-RTs) comprise a large portion of plant genomes, with massive repeat blocks distributed across the chromosomes. Eleocharis species have holocentric chromosomes, and show a positive correlation between chromosome numbers and the amount of nuclear DNA. To evaluate the role of LTR-RTs in karyotype diversity in members of Eleocharis (subgenus Eleocharis), the occurrence and location of different members of the Copia and Gypsy superfamilies were compared, covering interspecific variations in ploidy levels (considering chromosome numbers), DNA C-values and chromosomal arrangements.

Methods: The DNA C-value was estimated by flow cytometry. Genomes of Eleocharis elegans and E. geniculata were partially sequenced using Illumina MiSeq assemblies, which were a source for searching for conserved proteins of LTR-RTs. POL domains were used for recognition, comparing families and for probe production, considering different families of Copia and Gypsy superfamilies. Probes were obtained by PCR and used in fluorescence in situ hybridization (FISH) against chromosomes of seven Eleocharis species.

Key Results: A positive correlation between ploidy levels and the amount of nuclear DNA was observed, but with significant variations between samples with the same ploidy levels, associated with repetitive DNA fractions. LTR-RTs were abundant in E. elegans and E. geniculata genomes, with a predominance of Copia Sirevirus and Gypsy Athila/Tat clades. FISH using LTR-RT probes exhibited scattered and clustered signals, but with differences in the chromosomal locations of Copia and Gypsy. The diversity in LTR-RT locations suggests that there is no typical chromosomal distribution pattern for retrotransposons in holocentric chromosomes, except the CRM family with signals distributed along chromatids.

Conclusions: These data indicate independent fates for each LTR-RT family, including accumulation between and within chromosomes and genomes. Differential activity and small changes in LTR-RTs suggest a secondary role in nuclear DNA variation, when compared with ploidy changes.
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http://dx.doi.org/10.1093/aob/mcy066DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6070107PMC
August 2018

Comparative genome-wide characterization leading to simple sequence repeat marker development for Nicotiana.

BMC Genomics 2018 Jun 27;19(1):500. Epub 2018 Jun 27.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming, 650201, People's Republic of China.

Background: Simple sequence repeats (SSRs) are tandem repeats of DNA that have been used to develop robust genetic markers. These molecular markers are powerful tools for basic and applied studies such as molecular breeding. In the model plants in Nicotiana genus e.g. N. benthamiana, a comprehensive assessment of SSR content has become possible now because several Nicotiana genomes have been sequenced. We conducted a genome-wide SSR characterization and marker development across seven Nicotiana genomes.

Results: Here, we initially characterized 2,483,032 SSRs (repeat units of 1-10 bp) from seven genomic sequences of Nicotiana and developed SSR markers using the GMATA® software package. Of investigated repeat units, mono-, di- and tri-nucleotide SSRs account for 98% of all SSRs in Nicotiana. More complex SSR motifs, although rare, are highly variable between Nicotiana genomes. A total of 1,224,048 non-redundant Nicotiana (NIX) markers were developed, of which 99.98% are novel. An efficient and uniform genotyping protocol for NIX markers was developed and validated. We created a web-based database of NIX marker information including amplicon sizes of alleles in each genome for downloading and online analysis.

Conclusions: The present work constitutes the first deep characterization of SSRs in seven genomes of Nicotiana, and the development of NIX markers for these SSRs. Our online marker database and an efficient genotyping protocol facilitate the application of these markers. The NIX markers greatly expand Nicotiana marker resources, thus providing a useful tool for future research and breeding. We demonstrate a novel protocol for SSR marker development and utilization at the whole genome scale that can be applied to any lineage of organisms. The Tobacco Markers & Primers Database (TMPD) is available at http://biodb.sdau.edu.cn/tmpd/index.html.
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http://dx.doi.org/10.1186/s12864-018-4878-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6020451PMC
June 2018

A High-Quality Reference Genome for the Invasive Mosquitofish Using a Chicago Library.

G3 (Bethesda) 2018 05 31;8(6):1855-1861. Epub 2018 May 31.

Department of Genetics.

The western mosquitofish, , is a freshwater poecilid fish native to the southeastern United States but with a global distribution due to widespread human introduction. has been used as a model species for a broad range of evolutionary and ecological studies. We sequenced the genome of a male to facilitate genetic studies in diverse fields including invasion biology and comparative genetics. We generated Illumina short read data from paired-end libraries and proximity-ligation libraries. We obtained 54.9× coverage, N50 contig length of 17.6 kb, and N50 scaffold length of 6.65 Mb. Compared to two other species in the Poeciliidae family, has slightly fewer genes that have shorter total, exon, and intron length on average. Using a set of universal single-copy orthologs in fish genomes, we found 95.5% of these genes were complete in the assembly. The number of transposable elements in the assembly is similar to those of closely related species. The high-quality genome sequence and annotations we report will be valuable resources for scientists to map the genetic architecture of traits of interest in this species.
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http://dx.doi.org/10.1534/g3.118.200101DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5982815PMC
May 2018

Draft genome sequence of var. provides insights into the evolution of the tea genome and tea quality.

Proc Natl Acad Sci U S A 2018 05 20;115(18):E4151-E4158. Epub 2018 Apr 20.

BGI Genomics, BGI-Shenzhen, 518083 Shenzhen, China.

Tea, one of the world's most important beverage crops, provides numerous secondary metabolites that account for its rich taste and health benefits. Here we present a high-quality sequence of the genome of tea, var. (CSS), using both Illumina and PacBio sequencing technologies. At least 64% of the 3.1-Gb genome assembly consists of repetitive sequences, and the rest yields 33,932 high-confidence predictions of encoded proteins. Divergence between two major lineages, CSS and var. (CSA), is calculated to ∼0.38 to 1.54 million years ago (Mya). Analysis of genic collinearity reveals that the tea genome is the product of two rounds of whole-genome duplications (WGDs) that occurred ∼30 to 40 and ∼90 to 100 Mya. We provide evidence that these WGD events, and subsequent paralogous duplications, had major impacts on the copy numbers of secondary metabolite genes, particularly genes critical to producing three key quality compounds: catechins, theanine, and caffeine. Analyses of transcriptome and phytochemistry data show that amplification and transcriptional divergence of genes encoding a large acyltransferase family and leucoanthocyanidin reductases are associated with the characteristic young leaf accumulation of monomeric galloylated catechins in tea, while functional divergence of a single member of the glutamine synthetase gene family yielded theanine synthetase. This genome sequence will facilitate understanding of tea genome evolution and tea metabolite pathways, and will promote germplasm utilization for breeding improved tea varieties.
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http://dx.doi.org/10.1073/pnas.1719622115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5939082PMC
May 2018

Discovery of Lineage-Specific Genome Change in Rice Through Analysis of Resequencing Data.

Genetics 2018 06 19;209(2):617-626. Epub 2018 Apr 19.

Department of Genetics, University of Georgia, Athens, Georgia 30602

Genome comparisons provide information on the nature of genetic change, but such comparisons are challenged to differentiate the importance of the actual sequence change processes relative to the role of selection. This problem can be overcome by identifying changes that have not yet had the time to undergo millions of years of natural selection. We describe a strategy to discover accession-specific changes in the rice genome using an abundant resource routinely provided for many genome analyses, resequencing data. The sequence of the fully sequenced rice genome from variety Nipponbare was compared to the pooled (∼114×) resequencing data from 126 rice accessions to discover "Nipponbare-specific" sequences. Analyzing nonrepetitive sequences, 8504 "candidate" Nipponbare-specific changes were detected, of which around two-thirds are true novel sequence changes and the rest are predicted genome sequencing errors. Base substitutions outnumbered indels in this data set by > 28:1, with ∼8:5 bias toward transversions over transitions, and no transposable element insertions or excisions were observed. These results indicate that the strategy employed is effective for finding recent sequence changes, sequencing errors, and rare alleles in any organism that has both a reference genome sequence and a wealth of resequencing data.
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http://dx.doi.org/10.1534/genetics.118.300848DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5972431PMC
June 2018

Distinguishing friends, foes, and freeloaders in giant genomes.

Curr Opin Genet Dev 2018 04 12;49:49-55. Epub 2018 Mar 12.

Department of Genetics, University of Georgia, Athens, GA 30602, United States.

Most annotations of large eukaryotic genomes initially find transposable elements (TEs) and other repeats, then mask them so that subsequent efforts can be concentrated on the annotation and study of non-TE genes. However, TEs often contribute to host biology, and their community biologies are of intrinsic interest. This review discusses the challenges, rationale and technologies for comprehensive TE annotation in the commonly giant genomes of animals and plants. Complete discovery of the TEs in a fully sequenced genome is laborious, but feasible, with current strategies in the hands of a careful researcher. These deep TE studies have begun to provide important perspectives on how genomes evolve and the degree to which genome changes do and do not affect eukaryotic biology.
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http://dx.doi.org/10.1016/j.gde.2018.02.013DOI Listing
April 2018

Relationships between Gene Structure and Genome Instability in Flowering Plants.

Mol Plant 2018 03 17;11(3):407-413. Epub 2018 Feb 17.

State Key Laboratory of Tea Plant Biology and Utilization/Key Laboratory of Tea Biology and Processing, Ministry of Agriculture, Anhui Agricultural University, Hefei, Anhui 230036, People's Republic of China; Department of Genetics, University of Georgia, Athens, GA 30602, USA.

Flowering plant (angiosperm) genomes are exceptional in their variability with respect to genome size, ploidy, chromosome number, gene content, and gene arrangement. Gene movement, although observed in some of the earliest plant genome comparisons, has been relatively underinvestigated. We present herein a description of several interesting properties of plant gene and genome structure that are pertinent to the successful movement of a gene to a new location. These considerations lead us to propose a model that can explain the frequent success of plant gene mobility, namely that Small Insulated Genes Move Around (SIGMAR). The SIGMAR model is then compared with known processes for gene mobilization, and predictions of the SIGMAR model are formulated to encourage future experimentation. The overall results indicate that the frequent gene movement in angiosperm genomes is partly an outcome of the unusual properties of angiosperm genes, especially their small size and insulation from epigenetic silencing.
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http://dx.doi.org/10.1016/j.molp.2018.02.003DOI Listing
March 2018

Gene loss and genome rearrangement in the plastids of five Hemiparasites in the family Orobanchaceae.

BMC Plant Biol 2018 02 6;18(1):30. Epub 2018 Feb 6.

Department of Genetics, University of Georgia, Athens, GA, 30677, USA.

Background: The chloroplast genomes (plastome) of most plants are highly conserved in structure, gene content, and gene order. Parasitic plants, including those that are fully photosynthetic, often contain plastome rearrangements. These most notably include gene deletions that result in a smaller plastome size. The nature of gene loss and genome structural rearrangement has been investigated in several parasitic plants, but their timing and contributions to the adaptation of these parasites requires further investigation, especially among the under-studied hemi-parasites.

Results: De novo sequencing, assembly and annotation of the chloroplast genomes of five photosynthetic parasites from the family Orobanchaceae were employed to investigate plastome dynamics. Four had major structural rearrangements, including gene duplications and gene losses, that differentiated the taxa. The facultative parasite Aureolaria virginica had the most similar genome content to its close non-parasitic relative, Lindenbergia philippensis, with similar genome size and organization, and no differences in gene content. In contrast, the facultative parasite Buchnera americana and three obligate parasites in the genus Striga all had enlargements of their plastomes, primarily caused by expansion within the large inverted repeats (IRs) that are a standard plastome feature. Some of these IR increases were shared by multiple investigated species, but others were unique to particular lineages. Gene deletions and pseudogenization were also both shared and lineage-specific, with particularly frequent and independent loss of the ndh genes involved in electron recycling.

Conclusions: Five new plastid genomes were fully assembled and compared. The results indicate that plastome instability is common in parasitic plants, even those that retain the need to perform essential plastid functions like photosynthesis. Gene losses were slow and not identical across taxa, suggesting that different lineages had different uses or needs for some of their plastome gene content, including genes involved in some aspects of photosynthesis. Recent repeat region extensions, some unique to terminal species branches, were observed after the divergence of the Buchnera/Striga clade, suggesting that this otherwise rare event has some special value in this lineage.
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http://dx.doi.org/10.1186/s12870-018-1249-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5801802PMC
February 2018

Development and use of a switchgrass ( L.) transformation pipeline by the BioEnergy Science Center to evaluate plants for reduced cell wall recalcitrance.

Biotechnol Biofuels 2017 22;10:309. Epub 2017 Dec 22.

BioEnergy Science Center (BESC), Oak Ridge National Laboratory, Oak Ridge, TN 37831 USA.

Background: The mission of the BioEnergy Science Center (BESC) was to enable efficient lignocellulosic-based biofuel production. One BESC goal was to decrease poplar and switchgrass biomass recalcitrance to biofuel conversion while not affecting plant growth. A transformation pipeline (TP), to express transgenes or transgene fragments (constructs) in these feedstocks with the goal of understanding and decreasing recalcitrance, was considered essential for this goal. Centralized data storage for access by BESC members and later the public also was essential.

Results: A BESC committee was established to codify procedures to evaluate and accept genes into the TP. A laboratory information management system (LIMS) was organized to catalog constructs, plant lines and results from their analyses. One hundred twenty-eight constructs were accepted into the TP for expression in switchgrass in the first 5 years of BESC. Here we provide information on 53 of these constructs and the BESC TP process. Eleven of the constructs could not be cloned into an expression vector for transformation. Of the remaining constructs, 22 modified expression of the gene target. Transgenic lines representing some constructs displayed decreased recalcitrance in the field and publications describing these results are tabulated here. Transcript levels of target genes and detailed wall analyses from transgenic lines expressing six additional tabulated constructs aimed toward modifying expression of genes associated with wall structure (xyloglucan and lignin components) are provided. Altered expression of did not modify lignin content in transgenic plants. Simultaneous silencing of two was necessary to decrease G and S lignin monomer and total lignin contents, but this reduced plant growth.

Conclusions: A TP to produce plants with decreased recalcitrance and a LIMS for data compilation from these plants were created. While many genes accepted into the TP resulted in transgenic switchgrass without modified lignin or biomass content, a group of genes with potential to improve lignocellulosic biofuel yields was identified. Results from transgenic lines targeting xyloglucan and lignin structure provide examples of the types of information available on switchgrass lines produced within BESC. This report supplies useful information when developing coordinated, large-scale, multi-institutional reverse genetic pipelines to improve crop traits.
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http://dx.doi.org/10.1186/s13068-017-0991-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5740764PMC
December 2017

The Hardy Rubber Tree Genome Provides Insights into the Evolution of Polyisoprene Biosynthesis.

Mol Plant 2018 03 9;11(3):429-442. Epub 2017 Dec 9.

Key Laboratory of Biology and Genetic Resources of Rubber Tree, Ministry of Agriculture, Rubber Research Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou 571737, China. Electronic address:

Eucommia ulmoides, also called hardy rubber tree, is an economically important tree; however, the lack of its genome sequence restricts the fundamental biological research and applied studies of this plant species. Here, we present a high-quality assembly of its ∼1.2-Gb genome (scaffold N50 = 1.88 Mb) with at least 26 723 predicted genes for E. ulmoides, the first sequenced genome of the order Garryales, which was obtained using an integrated strategy combining Illumina sequencing, PacBio sequencing, and BioNano mapping. As a sister taxon to lamiids and campanulids, E. ulmoides underwent an ancient genome triplication shared by core eudicots but no further whole-genome duplication in the last ∼125 million years. E. ulmoides exhibits high expression levels and/or gene number expansion for multiple genes involved in stress responses and the biosynthesis of secondary metabolites, which may account for its considerable environmental adaptability. In contrast to the rubber tree (Hevea brasiliensis), which produces cis-polyisoprene, E. ulmoides has evolved to synthesize long-chain trans-polyisoprene via farnesyl diphosphate synthases (FPSs). Moreover, FPS and rubber elongation factor/small rubber particle protein gene families were expanded independently from the H. brasiliensis lineage. These results provide new insights into the biology of E. ulmoides and the origin of polyisoprene biosynthesis.
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http://dx.doi.org/10.1016/j.molp.2017.11.014DOI Listing
March 2018

Genome sequence of the progenitor of the wheat D genome Aegilops tauschii.

Nature 2017 11 15;551(7681):498-502. Epub 2017 Nov 15.

Department of Statistics, University of California, Davis, California, USA.

Aegilops tauschii is the diploid progenitor of the D genome of hexaploid wheat (Triticum aestivum, genomes AABBDD) and an important genetic resource for wheat. The large size and highly repetitive nature of the Ae. tauschii genome has until now precluded the development of a reference-quality genome sequence. Here we use an array of advanced technologies, including ordered-clone genome sequencing, whole-genome shotgun sequencing, and BioNano optical genome mapping, to generate a reference-quality genome sequence for Ae. tauschii ssp. strangulata accession AL8/78, which is closely related to the wheat D genome. We show that compared to other sequenced plant genomes, including a much larger conifer genome, the Ae. tauschii genome contains unprecedented amounts of very similar repeated sequences. Our genome comparisons reveal that the Ae. tauschii genome has a greater number of dispersed duplicated genes than other sequenced genomes and its chromosomes have been structurally evolving an order of magnitude faster than those of other grass genomes. The decay of colinearity with other grass genomes correlates with recombination rates along chromosomes. We propose that the vast amounts of very similar repeated sequences cause frequent errors in recombination and lead to gene duplications and structural chromosome changes that drive fast genome evolution.
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http://dx.doi.org/10.1038/nature24486DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7416625PMC
November 2017

New reference genome sequences of hot pepper reveal the massive evolution of plant disease-resistance genes by retroduplication.

Genome Biol 2017 11 1;18(1):210. Epub 2017 Nov 1.

Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, Seoul National University, Seoul, 08826, South Korea.

Background: Transposable elements are major evolutionary forces which can cause new genome structure and species diversification. The role of transposable elements in the expansion of nucleotide-binding and leucine-rich-repeat proteins (NLRs), the major disease-resistance gene families, has been unexplored in plants.

Results: We report two high-quality de novo genomes (Capsicum baccatum and C. chinense) and an improved reference genome (C. annuum) for peppers. Dynamic genome rearrangements involving translocations among chromosomes 3, 5, and 9 were detected in comparison between C. baccatum and the two other peppers. The amplification of athila LTR-retrotransposons, members of the gypsy superfamily, led to genome expansion in C. baccatum. In-depth genome-wide comparison of genes and repeats unveiled that the copy numbers of NLRs were greatly increased by LTR-retrotransposon-mediated retroduplication. Moreover, retroduplicated NLRs are abundant across the angiosperms and, in most cases, are lineage-specific.

Conclusions: Our study reveals that retroduplication has played key roles for the massive emergence of NLR genes including functional disease-resistance genes in pepper plants.
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http://dx.doi.org/10.1186/s13059-017-1341-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5664825PMC
November 2017

Integrating transcriptome and microRNA analysis identifies genes and microRNAs for AHO-induced systemic acquired resistance in N. tabacum.

Sci Rep 2017 10 2;7(1):12504. Epub 2017 Oct 2.

Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, 132 Lanhei Road, Kunming, 650201, P. R. China.

3-Acetonyl-3-hydroxyoxindole (AHO) induces systemic acquired resistance (SAR) in Nicotiana. However, the underlying molecular mechanism is not well understood. To understand the molecular regulation during SAR induction, we examined mRNA levels, microRNA (miRNA) expression, and their regulatory mechanisms in control and AHO-treated tobacco leaves. Using RNA-seq analysis, we identified 1,445 significantly differentially expressed genes (DEGs) at least 2 folds with AHO treatment. The DEGs significantly enriched in six metabolism pathways including phenylpropanoid biosynthesis, sesquiterpenoid and triterpenoid biosynthesis for protective cuticle and wax. Key DEGs including PALs and PR-10 in salicylic acid pathway involved in SAR were significantly regulated. In addition, we identified 403 miRNAs belonging to 200 miRNA families by miRNA sequencing. In total, AHO treatment led to 17 up- and 6 down-regulated at least 2 folds (Wald test, P < 0.05) miRNAs (DEMs), respectively. Targeting analysis implicated four DEMs regulating three DEGs involved in disease resistance, including miR156, miR172f, miR172g, miR408a, SPL6 and AP2. We concluded that both mRNA and miRNA regulation enhances AHO-induced SAR. These data regarding DEGs, miRNAs, and their regulatory mechanisms provide molecular evidence for the mechanisms involved in tobacco SAR, which are likely to be present in other plants.
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http://dx.doi.org/10.1038/s41598-017-12249-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5624873PMC
October 2017

Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments.

Nat Biotechnol 2017 Oct 18;35(10):969-976. Epub 2017 Sep 18.

Department of Ecogenomics and Systems Biology, University of Vienna, Vienna, Austria.

Pearl millet [Cenchrus americanus (L.) Morrone] is a staple food for more than 90 million farmers in arid and semi-arid regions of sub-Saharan Africa, India and South Asia. We report the ∼1.79 Gb draft whole genome sequence of reference genotype Tift 23DB-P1-P5, which contains an estimated 38,579 genes. We highlight the substantial enrichment for wax biosynthesis genes, which may contribute to heat and drought tolerance in this crop. We resequenced and analyzed 994 pearl millet lines, enabling insights into population structure, genetic diversity and domestication. We use these resequencing data to establish marker trait associations for genomic selection, to define heterotic pools, and to predict hybrid performance. We believe that these resources should empower researchers and breeders to improve this important staple crop.
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http://dx.doi.org/10.1038/nbt.3943DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6871012PMC
October 2017