ABSTRACT
Gene innovation plays an essential role in trait evolution. Rhizobial symbioses, the most important N2-fixing agent in agricultural systems that exists mainly in Leguminosae, is one of the most attractive evolution events. However, the gene innovations underlying Leguminosae root nodule symbiosis (RNS) remain largely unknown. Here, we investigated the gene gain event in Leguminosae RNS evolution through comprehensive phylogenomic analyses. We revealed that Leguminosae-gain genes were acquired by gene duplication and underwent a strong purifying selection. Kyoto Encyclopedia of Genes and Genomes analyses showed that the innovated genes were enriched in flavonoid biosynthesis pathways, particular downstream of chalcone synthase (CHS). Among them, Leguminosae-gain type â ¡ chalcone isomerase (CHI) could be further divided into CHI1A and CHI1B clades, which resulted from the products of tandem duplication. Furthermore, the duplicated CHI genes exhibited exon-intron structural divergences evolved through exon/intron gain/loss and insertion/deletion. Knocking down CHI1B significantly reduced nodulation in Glycine max (soybean) and Medicago truncatula; whereas, knocking down its duplication gene CHI1A had no effect on nodulation. Therefore, Leguminosae-gain type â ¡ CHI participated in RNS and the duplicated CHI1A and CHI1B genes exhibited RNS functional divergence. This study provides functional insights into Leguminosae-gain genetic innovation and sub-functionalization after gene duplication that contribute to the evolution and adaptation of RNS in Leguminosae.
ABSTRACT
The establishment of symbiotic interactions between leguminous plants and rhizobia requires complex cellular programming activated by Rhizobium Nod factors (NFs) as well as type III effector (T3E)-mediated symbiotic signaling. However, the mechanisms by which different signals jointly affect symbiosis are still unclear. Here we describe the mechanisms mediating the cross-talk between the broad host range rhizobia Sinorhizobium fredii HH103 T3E Nodulation Outer Protein L (NopL) effector and NF signaling in soybean. NopL physically interacts with the Glycine max Remorin 1a (GmREM1a) and the NFs receptor NFR5 (GmNFR5) and promotes GmNFR5 recruitment by GmREM1a. Furthermore, NopL and NF influence the expression of GmRINRK1, a receptor-like kinase (LRR-RLK) ortholog of the Lotus RINRK1, that mediates NF signaling. Taken together, our work indicates that S. fredii NopL can interact with the NF signaling cascade components to promote the symbiotic interaction in soybean.
Subject(s)
Bacterial Proteins , Gene Expression Regulation, Plant , Glycine max , Plant Proteins , Sinorhizobium fredii , Symbiosis , Glycine max/microbiology , Glycine max/metabolism , Plant Proteins/metabolism , Plant Proteins/genetics , Sinorhizobium fredii/metabolism , Sinorhizobium fredii/genetics , Bacterial Proteins/metabolism , Bacterial Proteins/genetics , Signal Transduction , Plant Root Nodulation/genetics , Plants, Genetically ModifiedABSTRACT
Flowering time and maturity are crucial agronomic traits that affect the regional adaptability of soybean plants. The development of soybean cultivars with early maturity adapted to longer days and colder climates of high latitudes is very important for ensuring normal ripening before frost begins. FUL belongs to the MADS-box transcription factor family and has several duplicated members in soybeans. In this study, we observed that overexpression of GmFULc in the Dongnong 50 cultivar promoted soybean maturity, while GmFULc knockout mutants exhibited late maturity. Chromatin immunoprecipitation sequencing (ChIP-seq) and RNA sequencing (RNA-seq) revealed that GmFULc could bind to the CArG, bHLH and homeobox motifs. Further investigation revealed that GmFULc could directly bind to the CArG motif in the promoters of the GmZTL3 and GmZTL4 genes. Overexpression of GmZTL4 promoted soybean maturity, whereas the ztl4 mutants exhibited delayed maturity. Moreover, we found that the cis element box 4 motif of the GmZTL4 promoter, a motif of light response elements, played an important role in controlling the growth period. Deletion of this motif shortened the growth period by increasing the expression levels of GmZTL4. Functional investigations revealed that short-day treatment promoted the binding of GmFULc to the promoter of GmZTL4 and inhibited the expression of E1 and E1Lb, ultimately resulting in the promotion of flowering and early maturation. Taken together, these findings suggest a novel photoperiod regulatory pathway in which GmFULc directly activates GmZTL4 to promote earlier maturity in soybean.
Subject(s)
Gene Expression Regulation, Plant , Glycine max , MADS Domain Proteins , Plant Proteins , Glycine max/genetics , Glycine max/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , MADS Domain Proteins/genetics , MADS Domain Proteins/metabolism , Promoter Regions, Genetic/genetics , Transcription Factors/metabolism , Transcription Factors/genetics , Transcription, Genetic , Plants, Genetically Modified/geneticsABSTRACT
Artificial domestication provided the original motivation to the blooming of agriculture, following with the dramatic change of the genetic background of crops and livestock. According to theory and technology upgradation that contributing to the omics, we appreciate using the pan-genome instead of single reference genome for crop study. By comparison and integration of multiple genomes under the guidance of pan-genome theory, we can estimate the genomic information range of a species, leading to a global understanding of its genetic diversity. Combining pan-genome with large size chromosomal structural variations, high throughput population resequencing, and multi-omics data, we can profoundly study the genetic basis behind species traits we focus on. Soybean is one of the most important commercial crops over the world. It is also essential to our food security. Dissecting the formation of genetic diversity and the causal loci of key agricultural traits of soybean will make the modern soybean breeding more efficiently. In this review, we summarize the core idea of pan-genome and clarified the characteristics of construction strategies of pan-genome such as de novo/mapping assembly, iterative assembly and graph-based genome. Then we used the soybean pan-genome work as a case study to introduce the general way to study pan-genome. We highlighted the contribution of structural variation (SV) to the evolution/domestication of soybean and its value in understanding the genetic bases of agronomy traits. By those, we approved the value of graph-based pan-genome for data integration and SV calculation. Future research directions are also discussed for crop genomics and data science.
Subject(s)
Genome, Plant , Glycine max , Plant Breeding , Sequence Analysis, DNA , GenomicsABSTRACT
Triterpenoid saponins, synthesized via the mevalonic acid (MVA) pathway in the cytoplasm, provide protection against pathogens and pests in plants and health benefits for humans. However, the mechanisms by which triterpenoid saponins are transported between cellular compartments remain uncharacterized. Here, we characterize a tonoplast localized multidrug and toxic compound extrusion transporter, GmMATE100 (encoded by Glyma.18G143700), from soybean (Glycine max L.). GmMATE100 is co-expressed with soyasaponin biosynthetic genes, and its expression was induced by MeJA treatment, which also led to soyasaponin accumulation in soybean roots. GmMATE100 efficiently transports multiple type-B soyasaponins as well as type-A soyasaponins with low affinity from the cytosol to the vacuole in a yeast system. The GmMATE100 loss-of-function mutant showed a significant decrease in type-A and type-B soyasaponin contents in soybean roots. This study not only characterized the first soybean triterpenoid saponin transporter but also provided new knowledge for the rational engineering of soyasaponin content and composition in soybean plants to modulate their levels within crop environments.
Subject(s)
Glycine max , Plant Proteins , Saponins , Vacuoles , Glycine max/metabolism , Glycine max/chemistry , Glycine max/genetics , Saponins/metabolism , Vacuoles/metabolism , Plant Proteins/metabolism , Plant Proteins/genetics , Biological Transport , Plant Roots/metabolism , Plant Roots/chemistry , Plant Roots/genetics , Gene Expression Regulation, PlantABSTRACT
Adzuki bean (Vigna angularis) is an important legume crop cultivated in over 30 countries worldwide. We developed a high-quality chromosome-level reference genome of adzuki bean cultivar Jingnong6 by combining PacBio Sequel long-read sequencing with short-read and Hi-C technologies. The assembled genome covers 97.8% of the adzuki bean genome with a contig N50 of approximately 16 Mb and a total of 32 738 protein-coding genes. We also generated a comprehensive genome variation map of adzuki bean by whole-genome resequencing (WGRS) of 322 diverse adzuki beans accessions including both wild and cultivated. Furthermore, we have conducted comparative genomics and a genome-wide association study (GWAS) on key agricultural traits to investigate the evolution and domestication. GWAS identified several candidate genes, including VaCycA3;1, VaHB15, VaANR1 and VaBm, that exhibited significant associations with domestication traits. Furthermore, we conducted functional analyses on the roles of VaANR1 and VaBm in regulating seed coat colour. We provided evidence for the highest genetic diversity of wild adzuki (Vigna angularis var. nipponensis) in China with the presence of the most original wild adzuki bean, and the occurrence of domestication process facilitating transition from wild to cultigen. The present study elucidates the genetic basis of adzuki bean domestication traits and provides crucial genomic resources to support future breeding efforts in adzuki bean.
Subject(s)
Genome, Plant , Genome-Wide Association Study , Vigna , Genome, Plant/genetics , Vigna/genetics , Chromosomes, Plant/genetics , Domestication , Genetic Variation , Genomics , Crops, Agricultural/genetics , PhenotypeABSTRACT
Stop codon readthrough (SCR) has important biological implications but remains largely uncharacterized. Here, we identify 1,009 SCR events in plants using a proteogenomic strategy. Plant SCR candidates tend to have shorter transcript lengths and fewer exons and splice variants than non-SCR transcripts. Mass spectrometry evidence shows that stop codons involved in SCR events can be recoded as 20 standard amino acids, some of which are also supported by suppressor tRNA analysis. We also observe multiple functional signals in 34 maize extended proteins and characterize the structural and subcellular localization changes in the extended protein of basic transcription factor 3. Furthermore, the SCR events exhibit non-conserved signature, and the extensions likely undergo protein-coding selection. Overall, our study not only characterizes that SCR events are commonly present in plants but also identifies the recoding plasticity of stop codons, which provides important insights into the flexibility of genetic decoding.
Subject(s)
Protein Biosynthesis , Proteins , Codon, Terminator/genetics , Proteins/genetics , Amino Acids/genetics , RNA, Transfer/geneticsSubject(s)
Drought Resistance , Glycine max , Glycine max/genetics , Plant Proteins/genetics , DroughtsABSTRACT
Soybean (Glycine max) is a crop with high demand for molybdenum (Mo) and typically requires Mo fertilization to achieve maximum yield potential. However, the genetic basis underlying the natural variation of Mo concentration in soybean and its impact on soybean agronomic performance is still poorly understood. Here, we performed a genome-wide association study (GWAS) to identify GmMOT1.1 and GmMOT1.2 that drive the natural variation of soybean Mo concentration and confer agronomic traits by affecting auxin synthesis. The soybean population exhibits five haplotypes of the two genes, with the haplotype 5 demonstrating the highest expression of GmMOT1.1 and GmMOT1.2, as well as the highest transport activities of their proteins. Further studies showed that GmMOT1.1 and GmMOT1.2 improve soybean yield, especially when cultivated in acidic or slightly acidic soil. Surprisingly, these two genes contribute to soybean growth by enhancing the activity of indole-3-acetaldehyde (IAAld) aldehyde oxidase (AO), leading to increased indole-3-acetic acid (IAA) synthesis, rather than being involved in symbiotic nitrogen fixation or nitrogen assimilation. Furthermore, the geographical distribution of five haplotypes in China and their correlation with soil pH suggest the potential significance of GmMOT1.1 and GmMOT1.2 in soybean breeding strategies.
Subject(s)
Glycine max , Molybdenum , Glycine max/genetics , Molybdenum/metabolism , Genome-Wide Association Study , Plant Breeding , Indoleacetic Acids/metabolism , SoilABSTRACT
Centromere repositioning refers to a de novo centromere formation at another chromosomal position without sequence rearrangement. This phenomenon was frequently encountered in both mammalian and plant species and has been implicated in genome evolution and speciation. To understand the dynamic of centromeres on soybean genome, we performed the pan-centromere analysis using CENH3-ChIP-seq data from 27 soybean accessions, including 3 wild soybeans, 9 landraces, and 15 cultivars. Building upon the previous discovery of three centromere satellites in soybean, we have identified two additional centromere satellites that specifically associate with chromosome 1. These satellites reveal significant rearrangements in the centromere structures of chromosome 1 across different accessions, consequently impacting the localization of CENH3. By comparative analysis, we reported a high frequency of centromere repositioning on 14 out of 20 chromosomes. Most newly emerging centromeres formed in close proximity to the native centromeres and some newly emerging centromeres were apparently shared in distantly related accessions, suggesting their emergence is independent. Furthermore, we crossed two accessions with mismatched centromeres to investigate how centromere positions would be influenced in hybrid genetic backgrounds. We found that a significant proportion of centromeres in the S9 generation undergo changes in size and position compared to their parental counterparts. Centromeres preferred to locate at satellites to maintain a stable state, highlighting a significant role of centromere satellites in centromere organization. Taken together, these results revealed extensive centromere repositioning in soybean genome and highlighted how important centromere satellites are in constraining centromere positions and supporting centromere function.
Subject(s)
Fabaceae , Glycine max , Centromere/genetics , Fabaceae/genetics , Glycine max/geneticsABSTRACT
Soyasaponins are major small molecules that accumulate in soybean (Glycine max) seeds. Among them, type-A soyasaponins, fully acetylated at the terminal sugar of their C22 sugar chain, are responsible for the bitter taste of soybean-derived foods. However, the molecular basis for the acetylation of type-A soyasaponins remains unclear. Here, we identify and characterize GmSSAcT1, encoding a BADH-type soyasaponin acetyltransferase that catalyzes three or four consecutive acetylations on type-A soyasaponins in vitro and in planta. Phylogenetic analysis and biochemical assays suggest that GmSSAcT1 likely evolved from acyltransferases present in leguminous plants involved in isoflavonoid acylation. Loss-of-function mutants of GmSSAcT1 exhibited impaired seed germination, which attribute to the excessive accumulation of null-acetylated type-A soyasaponins. We conclude that GmSSAcT1 not only functions as a detoxification gene for high accumulation of type-A soyasaponins in soybean seeds but is also a promising target for breeding new soybean varieties with lower bitter soyasaponin content.
Subject(s)
Glycine max , Taste , Glycine max/genetics , Germination/genetics , Acetyltransferases/genetics , Phylogeny , Seeds/genetics , Plant Breeding , SugarsABSTRACT
In eukaryotic cells, 3D genome plays an important role in the regulation of gene spatiotemporal expression, which is essential for the biological and developmental processes in a life cycle. In the past decade, the development of high-throughput technologies greatly enhances our ability to map the 3D genome organization, identifies multiple 3D genome structures, and investigates the functional role of 3D genome organization in gene regulation, which facilitates our understandings of cis-regulatory landscape and biological development. Comparing with the comprehensive analyses of 3D genome in mammals and model plants, the progress in soybean is much less. Future development and application of tools to precisely manipulate 3D genome structure at different levels will significantly strengthen the functional genome study and molecular breeding in soybean. Here, we review the recent progresses in 3D genome study and discuss future directions, which may help to improve soybean 3D functional genome study and molecular breeding.
ABSTRACT
Symbiotic nitrogen fixation (SNF) provides much of the N utilized by leguminous plants throughout growth and development. Legumes may simultaneously establish symbiosis with different taxa of microbial symbionts. Yet, the mechanisms used to steer associations toward symbionts that are most propitious across variations in soil types remain mysterious. Here, we demonstrate that GmRj2/Rfg1 is responsible for regulating symbiosis with multiple taxa of soybean symbionts. In our experiments, the GmRj2/Rfg1SC haplotype favored association with Bradyrhizobia, which is mostly distributed in acid soils, whereas the GmRj2/Rfg1HH haplotype and knockout mutants of GmRj2/Rfg1SC associated equally with Bradyrhizobia and Sinorhizobium. Association between GmRj2/Rfg1 and NopP, furthermore, appeared to be involved in symbiont selection. Furthermore, geographic distribution analysis of 1,821 soybean accessions showed that GmRj2/Rfg1SC haplotypes were enriched in acidic soils where Bradyrhizobia were the dominant symbionts, whereas GmRj2/Rfg1HH haplotypes were most prevalent in alkaline soils dominated by Sinorhizobium, and neutral soils harbored no apparent predilections toward either haplotype. Taken together, our results suggest that GmRj2/Rfg1 regulates symbiosis with different symbionts and is a strong determinant of soybean adaptability across soil regions. As a consequence, the manipulation of the GmRj2/Rfg1 genotype or application of suitable symbionts according to the haplotype at the GmRj2/Rfg1 locus might be suitable strategies to explore for increasing soybean yield through the management of SNF.
Subject(s)
Bradyrhizobium , Glycine max , Sinorhizobium , Glycine max/genetics , Glycine max/microbiology , Glycine max/physiology , Symbiosis , Nitrogen Fixation , Soil Microbiology , Soil/chemistry , Bradyrhizobium/physiology , Sinorhizobium/physiologyABSTRACT
The rhizosphere microbiota plays a critical and crucial role in plant health and growth, assisting plants in resisting adverse stresses, including soil salinity. Plastic film mulching is an important method to adjust soil properties and improve crop yield, especially in saline-alkali soil. However, it remains unclear whether and to what extent the association between these improvements and rhizosphere microbiota exists. Here, from a field survey and a greenhouse mesocosm experiment, we found that mulching plastic films on saline-alkali soil can promote the growth of soybeans in the field. Results of the greenhouse experiment showed that soybeans grew better in unsterilized saline-alkali soil than in sterilized saline-alkali soil under plastic film mulching. By detecting the variations in soil properties and analyzing the high-throughput sequencing data, we found that with the effect of film mulching, soil moisture content was effectively maintained, soil salinity was obviously reduced, and rhizosphere bacterial and fungal communities were significantly changed. Ulteriorly, correlation analysis methods were applied. The optimization of soil properties ameliorated the survival conditions of soil microbes and promoted the increase in relative abundance of potential beneficial microorganisms, contributing to the growth of soybeans. Furthermore, the classification of potential key rhizosphere microbial OTUs were identified. In summary, our study suggests the important influence of soil properties as drivers on the alteration of rhizosphere microbial communities and indicates the important role of rhizosphere microbiota in promoting plant performance in saline-alkali soil under plastic film mulching.
ABSTRACT
Tocopherols (vitamin E) play essential roles in human health because of their antioxidant activity, and plant-derived oils are the richest sources of tocopherols in the human diet. Although soybean (Glycine max) is one of the main sources of plant-derived oil and tocopherol in the world, the relationship between tocopherol and oil in soybean seeds remains unclear. Here, we focus on dissecting tocopherol metabolism with the long-term goal of increasing α-tocopherol content and soybean oil quality. We first collected tocopherol and fatty acid profiles in a soybean population (>800 soybean accessions) and found that tocopherol content increased during soybean domestication. A strong positive correlation between tocopherol and oil content was also detected. Five tocopherol pathway-related loci were identified using a metabolite genome-wide association study strategy. Genetic variations in three tocopherol pathway genes were responsible for total tocopherol content and composition in the soybean population through effects on enzyme activity, mainly caused by non-conserved amino acid substitution or changes in gene transcription level. Moreover, the fatty acid regulatory transcription factor GmZF351 directly activated tocopherol pathway gene expression, increasing both fatty acid and tocopherol contents in soybean seeds. Our study reveals the functional differentiation of tocopherol pathway genes in soybean populations and provides a framework for development of new soybean varieties with high α-tocopherol content and oil quality in seeds.
Subject(s)
Fatty Acids , Tocopherols , Humans , Tocopherols/analysis , Tocopherols/chemistry , Tocopherols/metabolism , Fatty Acids/metabolism , Glycine max/genetics , Glycine max/metabolism , alpha-Tocopherol/analysis , alpha-Tocopherol/metabolism , Genome-Wide Association Study , Plant Oils/metabolism , Seeds/geneticsSubject(s)
Glycine max , Multiomics , Glycine max/genetics , Genomics , Proteomics , Databases, FactualABSTRACT
BACKGROUND: High-order chromatin structure plays important roles in gene regulation. However, the diversity of the three-dimensional (3D) genome across plant accessions are seldom reported. RESULTS: Here, we perform the pan-3D genome analysis using Hi-C sequencing data from 27 soybean accessions and comprehensively investigate the relationships between 3D genomic variations and structural variations (SVs) as well as gene expression. We find that intersection regions between A/B compartments largely contribute to compartment divergence. Topologically associating domain (TAD) boundaries in A compartments exhibit significantly higher density compared to those in B compartments. Pan-3D genome analysis shows that core TAD boundaries have the highest transcription start site (TSS) density and lowest GC content and repeat percentage. Further investigation shows that non-long terminal repeat (non-LTR) retrotransposons play important roles in maintaining TAD boundaries, while Gypsy elements and satellite repeats are associated with private TAD boundaries. Moreover, presence and absence variation (PAV) is found to be the major contributor to 3D genome variations. Nevertheless, approximately 55% of 3D genome variations are not associated with obvious genetic variations, and half of them affect the flanking gene expression. In addition, we find that the 3D genome may also undergo selection during soybean domestication. CONCLUSION: Our study sheds light on the role of 3D genomes in plant genetic diversity and provides a valuable resource for studying gene regulation and genome evolution.
Subject(s)
Genome , Glycine max , Glycine max/genetics , Gene Expression Regulation , Retroelements , Genome, Plant , ChromatinABSTRACT
Recombination is crucial for crop breeding because it can break linkage drag and generate novel allele combinations. However, the high-resolution recombination landscape and its driving forces in soybean are largely unknown. Here, we constructed eight recombinant inbred line (RIL) populations and genotyped individual lines using the high-density 600K SoySNP array, which yielded a high-resolution recombination map with 5636 recombination sites at a resolution of 1.37 kb. The recombination rate was negatively correlated with transposable element density and GC content but positively correlated with gene density. Interestingly, we found that meiotic recombination was enriched at the promoters of active genes. Further investigations revealed that chromatin accessibility and active epigenetic modifications promoted recombination. Our findings provide important insights into the control of homologous recombination and thus will increase our ability to accelerate soybean breeding by manipulating meiotic recombination rate.