Rice Domestication Research Articles

Transposons are important contributors to gene expression variability under selection in rice populations

Transposable elements (TEs) are an important source of genome variability. Here, we analyze their contribution to gene expression variability in rice by performing a TE insertion polymorphism expression quantitative trait locus mapping using expression data from 208 varieties from the Oryza sativa ssp. indica and O. sativa ssp. japonica subspecies. Our data show that TE insertions are associated with changes of expression of many genes known to be targets of rice domestication and breeding. An important fraction of these insertions were already present in the rice wild ancestors, and have been differentially selected in indica and japonica rice populations. Taken together, our results show that small changes of expression in signal transduction genes induced by TE insertions accompany the domestication and adaptation of rice populations.

Transposons are important contributors to gene expression variability under selection in rice populations.

Transposable elements (TEs) are an important source of genome variability. Here, we analyze their contribution to gene expression variability in rice by performing a TE insertion polymorphism expression quantitative trait locus mapping using expression data from 208 varieties from the Oryza sativa ssp. indica and O. sativa ssp. japonica subspecies. Our data show that TE insertions are associated with changes of expression of many genes known to be targets of rice domestication and breeding. An important fraction of these insertions were already present in the rice wild ancestors, and have been differentially selected in indica and japonica rice populations. Taken together, our results show that small changes of expression in signal transduction genes induced by TE insertions accompany the domestication and adaptation of rice populations.

Gene Genealogy-Based Mutation Analysis Reveals Emergence of Aus, Tropical japonica, and Aromatic of Oryza sativa during the Later Stage of Rice Domestication.

Asian rice (Oryza sativa L.) has become a model for understanding gene functions and domestication in recent decades; however, its own diversification is still controversial. Although the division of indica and japonica and five subgroups (aus, indica (sensu stricto), japonica (sensu stricto), tropical japonica, and aromatic) are broadly accepted, how they are phylogenetically related is not transparent. To clarify their relationships, a sample of 121 diverse genes was chosen here from 12 Oryza genomes (two parental and ten O. sativa (Os)) in parallel to allow gene genealogy-based mutation (GGM) analysis. From the sample, 361 Os mutations were shared by two or more subgroups (referred to here as trans mutations) from 549 mutations identified at 51 Os loci. The GGM analysis and related tests indicates that aus diverged from indica at a time significantly earlier than when tropical japonica split from japonica. The results also indicate that aromatic was selected from hybrid progeny of aus and tropical japonica and that all five subgroups share a significant number of the early mutations identified previously. The results suggest that aus, tropical japonica, and aromatic emerged sequentially within the most recent 4-5 millennia of rice domestication after the split of indica and japonica.

Micro‐CT‐assisted determination of the shattering and non‐shattering phenotypes of charred rice spikelet bases from archaeological sites: a new methodological approach

AbstractThe selection of a non‐shattering phenotype is a pivotal change in the process of rice domestication. However, current research is heavily restricted by the preservation conditions of macro‐plant remains in early and middle Neolithic sites, as very limited well‐preserved rice spikelet bases could be retrieved. We present a non‐destructive method based on micro‐computed tomographic (CT) scanning, which could provide detailed visualization of the internal structures of charred spikelet bases and efficiently discriminate the shattering and non‐shattering phenotypes of rice spikelet bases according to the abundance of fusiform echinate phytoliths. It could be widely applied in different contexts, especially those poorly preserved specimens and tempers in pottery sherds, greatly improving our knowledge of rice domestication.

RNA-Seq Transcriptome Analysis and Evolution of OsEBS, a Gene Involved in Enhanced Spikelet Number per Panicle in Rice.

Spikelet number per panicle (SNP) is one of the most important yield components in rice. Rice ENHANCING BIOMASS AND SPIKELET NUMBER (OsEBS), a gene involved in improved SNP and yield, has been cloned from an accession of Dongxiang wild rice. However, the mechanism of OsEBS increasing rice SNP is poorly understood. In this study, the RNA-Seq technology was used to analyze the transcriptome of wildtype Guichao 2 and OsEBS over-expression line B102 at the heading stage, and analysis of the evolution of OsEBS was also conducted. A total of 5369 differentially expressed genes (DEGs) were identified between Guichao2 and B102, most of which were down-regulated in B102. Analysis of the expression of endogenous hormone-related genes revealed that 63 auxin-related genes were significantly down-regulated in B102. Gene Ontogeny (GO) enrichment analysis showed that the 63 DEGs were mainly enriched in eight GO terms, including auxin-activated signaling pathway, auxin polar transport, auxin transport, basipetal auxin transport, and amino acid transmembrane transport, most of which were directly or indirectly related to polar auxin transport. Kyoto Encyclopedia of Genes and Genomes (KEGG) metabolic pathway analysis further verified that the down-regulated genes related to polar auxin transport had important effects on increased SNP. Analysis of the evolution of OsEBS found that OsEBS was involved in the differentiation of indica and japonica, and the differentiation of OsEBS supported the multi-origin model of rice domestication. Indica (XI) subspecies harbored higher nucleotide diversity than japonica (GJ) subspecies in the OsEBS region, and XI experienced strong balancing selection during evolution, while selection in GJ was neutral. The degree of genetic differentiation between GJ and Bas subspecies was the smallest, while it was the highest between GJ and Aus. Phylogenetic analysis of the Hsp70 family in O. sativa, Brachypodium distachyon, and Arabidopsis thaliana indicated that changes in the sequences of OsEBS were accelerated during evolution. Accelerated evolution and domain loss in OsEBS resulted in neofunctionalization. The results obtained from this study provide an important theoretical basis for high-yield rice breeding.

Asymmetric variation in DNA methylation during domestication and de-domestication of rice.

Hundreds of plant species have been domesticated to feed human civilization, while some crops have undergone de-domestication into agricultural weeds, threatening global food security. To understand the genetic and epigenetic basis of crop domestication and de-domestication, we generated DNA methylomes from 95 accessions of wild rice (Oryza rufipogon L.), cultivated rice (Oryza sativa L.) and weedy rice (O. sativa f. spontanea). We detected a significant decrease in DNA methylation over the course of rice domestication but observed an unexpected increase in DNA methylation through de-domestication. Notably, DNA methylation changes occurred in distinct genomic regions for these 2 opposite stages. Variation in DNA methylation altered the expression of nearby and distal genes through affecting chromatin accessibility, histone modifications, transcription factor binding, and the formation of chromatin loops, which may contribute to morphological changes during domestication and de-domestication of rice. These insights into population epigenomics underlying rice domestication and de-domestication provide resources and tools for epigenetic breeding and sustainable agriculture.

Multicropping Pattern Reveals Human Adaptation at the Wanbei Site (ca. 5.7–4.4 ka cal. BP) in the Middle and Lower Huai River Valley, China

The middle and lower Huai River Valley, located between the Yangtze and Yellow Rivers, was a key transitional zone for the northward spread of rice and southward migration of millet agriculture in central-eastern China during the Holocene. Knowing when millets spread here, how they were combined with rice in mixed farming, the reasons for their spread, and the temporal variation of cropping patterns is of crucial significance to the development of our understanding of ancient adaptation strategies adopted by human societies in response to climatic and cultural changes. Focusing on crops, phytolith analyses of the soil samples, in tandem with radiocarbon dating from the Wanbei site, reveal evidence of a multicropping pattern of combining rice (Oryza sative), broomcorn millet (Panicum miliaceum), and foxtail millet (Setaria italica) during the Dawenkou culture period between 5720 and 4426 cal. BP in the middle and lower Huai River Valley, China. The data show that rice was always the principal crop of the pattern, and that domesticated rice was developed during the early and middle Dawenkou culture periods. However, its domestication rate became lower during the late Dawenkou culture period. Broomcorn millet and foxtail millet with domesticated traits appeared only in lower proportions of the total produced throughout the period. The proportions of rice and foxtail millet increased slightly, while the proportions of broomcorn millet decreased over time. Finally, the formation of the multicropping pattern at Wanbei may have been primarily influenced by both the warm and wet climatic environment and the cultural exchange and communication between the Haidai region and the middle and lower Huai River Valley during the Dawenkou culture period. The findings in this paper may not only contribute to mapping the spatiotemporal route for the northward expansion of rice agriculture and southward spread of millet agriculture, but also assist in understanding the human adaptation strategies employed in eastern China during the Holocene.

Inferring Historical Introgression with Deep Learning.

Resolving phylogenetic relationships among taxa remains a challenge in the era of big data due to the presence of genetic admixture in a wide range of organisms. Rapidly developing sequencing technologies and statistical tests enable evolutionary relationships to be disentangled at a genome-wide level, yet many of these tests are computationally intensive and rely on phased genotypes, large sample sizes, restricted phylogenetic topologies, or hypothesis testing. To overcome these difficulties, we developed a deep learning-based approach, named ERICA, for inferring genome-wide evolutionary relationships and local introgressed regions from sequence data. ERICA accepts sequence alignments of both population genomic data and multiple genome assemblies, and efficiently identifies discordant genealogy patterns and exchanged regions across genomes when compared with other methods. We further tested ERICA using real population genomic data from Heliconius butterflies that have undergone adaptive radiation and frequent hybridization. Finally, we applied ERICA to characterize hybridization and introgression in wild and cultivated rice, revealing the important role of introgression in rice domestication and adaptation. Taken together, our findings demonstrate that ERICA provides an effective method for teasing apart evolutionary relationships using whole genome data, which can ultimately facilitate evolutionary studies on hybridization and introgression.

OsMADS17 simultaneously increases grain number and grain weight in rice

During the processes of rice domestication and improvement, a trade-off effect between grain number and grain weight was a major obstacle for increasing yield. Here, we identify a critical gene COG1, encoding the transcription factor OsMADS17, with a 65-bp deletion in the 5′ untranslated region (5′ UTR) presented in cultivated rice increasing grain number and grain weight simultaneously through decreasing mRNA translation efficiency. OsMADS17 controls grain yield by regulating multiple genes and that the interaction with one of them, OsAP2-39, has been characterized. Besides, the expression of OsMADS17 is regulated by OsMADS1 directly. It indicates that OsMADS1-OsMADS17-OsAP2-39 participates in the regulatory network controlling grain yield, and downregulation of OsMADS17 or OsAP2-39 expression can further improve grain yield by simultaneously increasing grain number and grain weight. Our findings provide insights into understanding the molecular basis co-regulating rice yield-related traits, and offer a strategy for breeding higher-yielding rice varieties.

Holocene coastal sedimentary evolution and neolithic human adaption in response to sea level changes in the Palaeo-Taihu valley, East China

The neolithic human-land relationship in the eastern coastal plain of China, interlinked sedimentary evolution and sea level changes, has been central to numerous studies. Here, we focus on the evolution of the sedimentary environment and its impacts on human activity in the Palaeo-Taihu valley (PTV) within the northern wing of Hangzhou Bay in response to post-glacial sea level rise. We employ multi-proxy analyses (lithology, AMS 14C, grain size, elements, TOC, and microfossil) on a new sediment core (WZ05) of comparatively analyze a series of previous radiocarbon-dated cores. Our results indicate that since the last deglaciation, the sedimentary environment of Core WZ05 has undergone the floodplain, upper tidal flat, estuary, upper tidal flat, coastal marsh, and fluvial plain, respectively. Regional cores comparisons display three stages: (1) A late Pleistocene incised valley (older than 9600 cal yr BP) dominated by terrestrial deposits accompanied by pottery sherds and rice phytoliths revealing that human activity on the floodplain can be dated to ca. 10600-10300 cal yr BP; (2) An early-mid Holocene transgression stage (9600-7800 cal yr BP) resulted from rapid sea level rise, causing widespread seawater inundation of the floodplain which interrupted early human activity. The transgression maximum during 8000-7800 cal yr BP was marked by the highest sedimentation rates and the coexistence of deep and shallow water species of foraminifera, corresponding to the appearance of a semi-enclosed estuary; (3) Finally, mid-late Holocene terrestrial deposits are the response to a slower sea-level rise and the seaward migration of the coast as the sediment supply exceeded sea level rise at 7800 cal yr BP. Tidal flats and coastal marshes dominated the PTV until 6500 cal yr BP, thereafter sediments continue to fill the PTV such that it develops into a subaerial plain. The reappearance of a freshwater environment since ∼ 7600 cal yr BP allowed the recovery of rice cultivation in the region. Saltwater deposits interspersed with terrestrial deposits between 7000-6500 cal yr BP probably reflect marine inundation during storm events and would have depressed rice domestication.

Advances in Rice Seed Shattering.

Seed shattering is an important trait that wild rice uses to adapt to the natural environment and maintain population reproduction, and weedy rice also uses it to compete with the rice crop. The loss of shattering is a key event in rice domestication. The degree of shattering is not only one of the main reasons for rice yield reduction but also affects its adaptability to modern mechanical harvesting methods. Therefore, it is important to cultivate rice varieties with a moderate shattering degree. In this paper, the research progress on rice seed shattering in recent years is reviewed, including the physiological basis, morphological and anatomical characteristics of rice seed shattering, inheritance and QTL/gene mapping of rice seed shattering, the molecular mechanism regulating rice seed shattering, the application of seed-shattering genes, and the relationship between seed-shattering genes and domestication.

Detection of novel loci involved in non-seed-shattering behaviour of an indica rice cultivar, Oryza sativa IR36

Asian rice (Oryza sativa) was domesticated from O. rufipogon, and reduced seed-shattering behaviour was selected to increase yields. Two seed-shattering loci, qSH3 and sh4, are involved in reducing seed shattering in both japonica and indica rice cultivars, while qSH1 and qCSS3 are likely specific to japonica cultivars. In indica cultivars, qSH3 and sh4 fail to explain the degree of seed shattering, as an introgression line (IL) of O. rufipogon W630 carrying domesticated alleles at qSH3 and sh4 still showed seed shattering. Here we analysed differences in seed-shattering degree between the IL and the indica cultivar IR36. The values for grain detachment in the segregating population between the IL and IR36 were continuous. Based on QTL-seq analysis using the BC1F2 population between the IL and IR36, we detected two novel loci, qCSS2 and qCSS7 (QTLs for the Control of Seed Shattering in rice on chromosomes 2 and 7), which contributed to the reduced seed shattering in IR36. We further investigated the genetic interaction of qCSS2 and qCSS7 under the presence of qSH3 and sh4 mutations in O. rufipogon W630 and found that IL carrying IR36 chromosomal segments covering all four loci are required to explain seed-shattering degree in IR36. Since qCSS2 and qCSS7 were not detected in previous studies on seed shattering in japonica, their control may be specific to indica cultivars. Therefore, they are important to understanding the history of rice domestication as well as to adjusting the seed-shattering degree of indica cultivars to maximise their yield.

The Lesson Learned from the Unique Evolutionary Story of Avirulence Gene AvrPii of Magnaporthe oryzae.

Blast, caused by Magnaporthe oryzae, is one of the most destructive diseases affecting rice production. Understanding population dynamics of the pathogen's avirulence genes is pre-required for breeding and then deploying new cultivars carrying promising resistance genes. The divergence and population structure of AvrPii was dissected in the populations of southern (Guangdong, Hunan, and Guizhou) and northern (Jilin, Liaoning, and Heilongjiang) China, via population genetic and evolutionary approaches. The evolutionary divergence between a known haplotype AvrPii-J and a novel one AvrPii-C was demonstrated by haplotype-specific amplicon-based sequencing and genetic transformation. The different avirulent performances of a set of seven haplotype-chimeric mutants suggested that the integrity of the full-length gene structures is crucial to express functionality of individual haplotypes. All the four combinations of phenotypes/genotypes were detected in the three southern populations, and only two in the northern three, suggesting that genic diversity in the southern region was higher than those in the northern one. The population structure of the AvrPii family was shaped by balancing, purifying, and positive selection pressures in the Chinese populations. The AvrPii-J was recognized as the wild type that emerged before rice domestication. Considering higher frequencies of avirulent isolates were detected in Hunan, Guizhou, and Liaoning, the cognate resistance gene Pii could be continuously used as a basic and critical resistance resource in such regions. The unique population structures of the AvrPii family found in China have significant implications for understanding how the AvrPii family has kept an artful balance and purity among its members (haplotypes) those keenly interact with Pii under gene-for-gene relationships. The lesson learned from case studies on the AvrPii family is that much attention should be paid to haplotype divergence of target gene.

Serving red rice beer to the ancestors ca. 9000 years ago at Xiaohuangshan early Neolithic site in south China

Microfossil analyses of three early Neolithic pottery vessels from Xiaohuangshan, a middle Shangshan culture site in Zhejiang (ca. 9000–8500 cal. BP), revealed the earliest evidence of red rice beer brewing in China. This fermentation method involved the preparation of qu starter with Monascus mold, rice, and probably herbs; the brewing ingredients may have included mainly rice, together with Job’s tears, acorn, and lily bulb; and globular jars were used as fermenters. The dregs of the red beer may have been used for cooking with solid foods and served with them on plates at feasts. The globular jar analyzed was a part of the grave goods assemblage, suggesting that alcoholic beverages were sacrificial offerings to the dead ancestors. This mortuary practice, which involved rice-based fermented beverages, emerged in the early stage of rice cultivation under the wet-warm climatic conditions during the early Holocene, shedding new light on the driving forces of the origin and dispersal of rice domestication in China.

A leaf-emanated signal orchestrates grain size and number in response to maternal resources.

In plants, variations in seed size and number are outcomes of different reproductive strategies. Both traits are often environmentally influenced, suggesting that a mechanism exists to coordinate these phenotypes in response to available maternal resources. Yet, how maternal resources are sensed and influence seed size and number is largely unknown. Here, we report a mechanism that senses maternal resources and coordinates grain size and number in the wild rice Oryza rufipogon, a wild progenitor of Asian cultivated rice. We showed that FT-like 9 (FTL9) regulates both grain size and number and that maternal photosynthetic assimilates induce FTL9 expression in leaves to act as a long-range signal that increases grain number and reduces size. Our findings highlight a strategy that benefits wild plants to survive in a fluctuating environment. In this strategy, when maternal resources are sufficient, wild plants increase their offspring number while preventing an increase in offspring size by the action of FTL9, which helps expand their habitats. In addition, we found that a loss-of-function allele (ftl9) is prevalent among wild and cultivated populations, offering a new scenario in the history of rice domestication.

The legacies of the "Father of Hybrid Rice" and the seven representative achievements of Chinese rice research: A pioneering perspective towards sustainable development.

The "Father of Hybrid Rice", Yuan Longping, created high-yield hybrid rice that can feed tens of millions of people annually. The research achievements of Yuan and his team on low cadmium-accumulating rice and sea rice, in addition to hybrid rice, as well as those of a large number of Chinese scientists engaged in rice research in other six areas, including the rice genome, purple endosperm rice, de novo domestication of tetraploid rice, perennial rice, rice blast disease, and key genes for high nitrogen use efficiency, play an important role in promoting the realization of the United Nations Sustainable Development Goals 2 and 12. The purpose of this review is not to elaborate on the details of each research, but to innovatively summarize the significance and inspiration of these achievements to ensure global food security and achieve sustainable agriculture. In the future, cultivating new rice varieties through modern biotechnology, such as genome editing, will not only reduce hunger, but potentially reduce human-land conflicts, improve the environment, and mitigate climate change.

<italic>De novo</italic> domestication and preliminary cultivar development of sand rice (<italic>Agriophyllum squarrosum</italic>), a sand dune pioneer species

<p indent="0mm">The comprehensive utilization of desert plants and sandy land resources is of far-reaching significance to the eco-civilization progress and food security in the arid region of northern China. The pioneer species <italic>Agriophyllum squarrosum</italic> is broadly distributed on the mobile sand dunes in the arid and semi-arid areas of northern China. Its seed, also called sand rice, has well-balanced nutritional values and has been consumed for more than <sc>1300 years.</sc> In 2010, our group first initiated the domestication research of sand rice by investigating the various historical literature and food consuming records of sand rice. Genetic modification and breeding are currently dependent on natural populations and artificial mutagenesis. A few modified lines with better agronomic traits have been initially isolated, laying a material foundation for further cultivation evaluation in different areas and cultivar declaration. However, the speed domestication of sand rice still requires systematically analyzing phenotypic variation among different germplasms, the establishment of a genetic transformation system, and isolating elite lines with a synchronous germination rate and strong seedling vigor.

Lost genome segments associate with trait diversity during rice domestication

BackgroundDNA mutations of diverse types provide the raw material required for phenotypic variation and evolution. In the case of crop species, previous research aimed to elucidate the changing patterns of repetitive sequences, single-nucleotide polymorphisms (SNPs), and small InDels during domestication to explain morphological evolution and adaptation to different environments. Additionally, structural variations (SVs) encompassing larger stretches of DNA are more likely to alter gene expression levels leading to phenotypic variation affecting plant phenotypes and stress resistance. Previous studies on SVs in rice were hampered by reliance on short-read sequencing limiting the quantity and quality of SV identification, while SV data are currently only available for cultivated rice, with wild rice largely uncharacterized. Here, we generated two genome assemblies for O. rufipogon using long-read sequencing and provide insights on the evolutionary pattern and effect of SVs on morphological traits during rice domestication.ResultsIn this study, we identified 318,589 SVs in cultivated and wild rice populations through a comprehensive analysis of 13 high-quality rice genomes and found that wild rice genomes contain 49% of unique SVs and an average of 1.76% of genes were lost during rice domestication. These SVs were further genotyped for 649 rice accessions, their evolutionary pattern during rice domestication and potential association with the diversity of important agronomic traits were examined. Genome-wide association studies between these SVs and nine agronomic traits identified 413 candidate causal variants, which together affect 361 genes. An 824-bp deletion in japonica rice, which encodes a serine carboxypeptidase family protein, is shown to be associated with grain length.ConclusionsWe provide relatively accurate and complete SV datasets for cultivated and wild rice accessions, especially in TE-rich regions, by comparing long-read sequencing data for 13 representative varieties. The integrated rice SV map and the identified candidate genes and variants represent valuable resources for future genomic research and breeding in rice.

Analysis of Domestication Loci in Wild Rice Populations.

The domestication syndrome is defined as a collection of domestication-related traits that have undergone permanent genetic changes during the domestication of cereals. Australian wild rice populations have not been exposed to gene flow from domesticated rice populations. A high level of natural variation of the sequences at domestication loci (e.g., seed shattering, awn development, and grain size) was found in Australian AA genome wild rice from the primary gene pool of rice. This natural variation is much higher than that found in Asian cultivated rice and wild Asian rice populations. The Australian Oryza meridionalis populations exhibit a high level of homozygous polymorphisms relative to domesticated rice, inferring the fixation of distinct wild and domesticated alleles. Alleles of the seed shattering genes (SH4/SHA1 and OsSh1/SH1) present in the shattering-prone O. meridionalis populations are likely to be functional, while the dysfunctional alleles of these seed shattering genes are found in domesticated rice. This confirms that unlike Asian wild rice populations, Australian wild rice populations have remained genetically isolated from domesticated rice, retaining pre-domestication alleles in their wild populations that uniquely allow the impact of domestication on the rice genome to be characterized. This study also provides key information about the domestication loci in Australian wild rice populations that will be valuable in the utilization of these genetic resources in crop improvement and de novo domestication.

Regulator of Awn Elongation 3, an E3 ubiquitin ligase, is responsible for loss of awns during African rice domestication

Two species of rice have been independently domesticated from different ancestral wild species in Asia and Africa. Comparison of mutations that underlie phenotypic and physiological alterations associated with domestication traits in these species gives insights into the domestication history of rice in both regions. Asian cultivated rice, Oryza sativa, and African cultivated rice, Oryza glaberrima, have been modified and improved for common traits beneficial for humans, including erect plant architecture, nonshattering seeds, nonpigmented pericarp, and lack of awns. Independent mutations in orthologous genes associated with these traits have been documented in the two cultivated species. Contrary to this prevailing model, selection for awnlessness targeted different genes in O. sativa and O. glaberrima. We identify Regulator of Awn Elongation 3 (RAE3) a gene that encodes an E3 ubiquitin ligase and is responsible for the awnless phenotype only in O. glaberrima. A 48-bp deletion may disrupt the substrate recognition domain in RAE3 and diminish awn elongation. Sequencing analysis demonstrated low nucleotide diversity in a ~600-kb region around the derived rae3 allele on chromosome 6 in O. glaberrima compared with its wild progenitor. Identification of RAE3 sheds light on the molecular mechanism underlying awn development and provides an example of how selection on different genes can confer the same domestication phenotype in Asian and African rice.