Research by Dorian Fuller, UCL colleagues and collaborative partners is being featured in a special issue of the Proceedings of the National Academy of Sciences of the United States of America (PNAS). The papers are part of a collection entitled: "The Modern View of Domestication", edited by Greger Larson and Dolores R. Piperno, Special Feature of The Proceedings of the National Academy of Sciences, USA (29 April 2014). Early Edition online content is available now via the links below
Genetic improvements in plant breeding programs in local regions have led to the development of new cultivars with specific agronomic traits under environmental conditions and generated the unique genetic structures of local populations. Understanding historical changes in genome structures and phenotypic characteristics within local populations may be useful for identifying profitable genes and/or genetic resources and the creation of new gene combinations in plant breeding programs. In the present study, historical changes were elucidated in genome structures and phenotypic characteristics during 100-year rice breeding programs in Hokkaido, the northern limit of rice cultivation in the world. We selected 63 rice cultivars to represent the historical diversity of this local population from landraces to the current breeding lines. The results of the phylogenetic analysis demonstrated that these cultivars clearly differentiated into six groups over the history of rice breeding programs. Significant differences among these groups were detected in five of the seven traits, indicating that the differentiation of the Hokkaido rice population into these groups was correlated with these phenotypic changes. These results demonstrated that breeding practices in Hokkaido have created new genetic structures for adaptability to specific environmental conditions and breeding objectives. They also provide a new strategy for rice breeding programs in which such unique genes in local populations in the world can explore the genetic potentials of the local populations.
The Indian Ocean has long been a forum for contact, trade and the transfer of goods, technologies and ideas between geographically distant groups of people. Another, less studied, outcome of expanding maritime connectivity in the region is the translocation of a range of species of plants and animals, both domestic and wild. A significant number of these translocations can now be seen to involve Africa, either providing or receiving species, suggesting that Africa’s role in the emergence of an increasingly connected Indian Ocean world deserves more systematic consideration. While the earliest international contacts with the East African coast remain poorly understood, in part due to a paucity of archaeobotanical and zooarchaeological studies, some evidence for early African coastal activity is provided by the discovery of early hunter-gatherer sites on offshore islands, and, possibly, by the translocation of wild animals among these islands, and between them and the mainland. From the seventh century, however, clear evidence for participation in the Indian Ocean world emerges, in the form of a range of introduced species, including commensal and domestic animals, and agricultural crops. New genetic studies demonstrate that the flow of species to the coast is complex, with more than one source frequently indicated. The East African coast and Madagascar appear to have been significant centres of genetic admixture, drawing upon Southeast Asian, South Asian and Middle Eastern genetic varieties, and sometimes yielding unique hybrid species. The biological patterns reflect a deeply networked trade and contact situation, and support East Africa’s key role in the events and transformations of the early Indian Ocean world.
Dorian Q Fuller's insight:
Includes an updated review of the evidence for the arrival of Asian rice in Africa
Rice (Oryza sativa L.) is important to food security and is also an excellent model plant for numerous cereal crops. A functional genomics study in rice includes characterization of the expression dynamics of genes by quantitative real-time PCR (qPCR) analysis; this is a significant key for developing rice varieties that perform well in the face of adverse climate change. The qPCR analysis requires the use of appropriate reference genes in order to make any quantitative interpretations meaningful. Here, the new potential reference genes were selected from a huge public database of rice microarray experiments. The expression stability of 14 candidates and 4 conventional reference genes was validated by geNormPLUS and NormFinder software. Seven candidates are superior to the conventionally used reference genes in qPCR and three genes can be used reliably for quantitating the expression of genes involved in abiotic stress responses. These high-quality references EP (LOC_Os05g08980), HNR (LOC_Os01g71770), and TBC(LOC_Os09g34040) worked very well in three indica genotypes and one japonica genotype. One ofindica genotypes including the Jasmine rice, KDML105 developed in Thailand for which no reference genes have been reported until now.
Rice is a model system for crop genomics studies. Much of the early work on rice genomics focused on analyzing genome-wide genetic variation to further understand rice gene functions in agronomic traits and to generate data and resources for rice research. The advent of next-generation high-throughput DNA sequencing technologies and the completion of high-quality reference genome sequences have enabled the development of sequencing-based genotyping and genome-wide association studies (GWAS) that have significantly advanced rice genetics research. This has led to the emergence of a new era of rice genomics aimed at bridging the knowledge gap between genotype and phenotype in rice. These technologies have also led to pyramid breeding through genomics-assisted selection, which will be useful in breeding elite varieties suitable for sustainable agriculture. Here, we review the recent advances in rice genomics and discuss the future of this line of research.
Rice can be cultivated in a range of arable systems, including upland rainfed, lowland rainfed or irrigated, flooded or décrue, and deep water cultivation. These agricultural regimes represent ecosystems controlled to large degree by agricultural practices, and can be shown to produce different weed flora assemblages. In order to reconstruct early rice cultivation systems it is necessary to better establish how ancient rice farming practices may be seen using archaeobotanical data. This paper focuses on using modern analogue phytolith assemblages of associated crop weeds found within cultivation regimes, as well as in wild rice stands (unplanted stands of Oryza nivara or O. rufipogon), as a means of interpreting archaeobotanical assemblages. Rice weeds and sediment samples have been recorded and collected from a range of arable systems and wild stands in India. The husks, leaves and culms of associated weeds were processed for phytolith reference samples, and sediment samples were processed for phytoliths in order to establish patterns identifiable to specific systems. The preliminary results of the phytolith analysis of samples from these modern fields demonstrate that phytolith assemblage statistics show correlation with variation in rice cultivation systems on the basis of differences in environmental conditions and regimes, with wetness being one major factor. Analysis of phytoliths from archaeological samples from contrasting systems in Neolithic China and India demonstrate how this method can be applied to separate archaeological regions and periods based on inferred differences in past agricultural practices, identifying wet cultivation systems in China, dry millet-dominated agriculture of north China and rainfed/dry rice in Neolithic India.
Dorian Q Fuller's insight:
We present a new methodology for identifying ancient rice arable systems.
We create modern analogues of phytolith assemblages of rice weeds from modern fields.
These analogues are used as models to understand archaeobotanical samples.
We present an analysis of different systems from Neolithic India and China.
Improvement of rice eating quality is an important objective in current breeding programs. In this study, 130 rice accessions of diverse origin were genotyped using 170 SSR markers to identify marker–trait associations with physicochemical traits on eating quality. Analysis of population structure revealed four subgroups in the population. Linkage disequilibrium (LD) patterns and distributions are of fundamental importance for genome-wide mapping associations. The mean r 2value for all intrachromosomal loci pairs was 0.0940. LD between linked markers decreased with distance. Marker–trait associations were investigated using the unified mixed-model approach, considering both population structure (Q) and kinship (K). In total, 101 marker–trait associations (p < 0.05) were identified using 52 different SSR markers covering 12 chromosomes. The results suggest that association mapping in rice is a viable alternative to quantitative trait loci mapping, and detection of new marker–trait associations associated with rice eating quality will also provide important information for marker-assisted breeding and functional analysis of rice grain quality.
Wednesday evening the College of Humanities and Social Sciences welcomed world-renowned archaeobotanist Dorian Fuller to ASU for his lecture, “The Archaeobotany of Rice: From Domestication to Global Warming.”...
During the diversification of cultivated rice after domestication, rice was grown in diverse geographic regions using genetic variations attributed to the combination of alleles in loci for adaptability to various environmental conditions. To elucidate the key gene for adaptation in rice cultivars to the northern limit of rice cultivation, we conducted genetic analyses of heading date using extremely early-heading cultivars. The Hd5 gene controlling heading date (flowering time) generated variations in heading date among cultivars adapted to Hokkaido, where is the northernmost region of Japan and one of the northern limits of rice cultivation in the world. The association of the Hd5 genotype with heading date and genetical analysis clearly showed that the loss-of-function Hd5 has an important role in exhibiting earlier heading among a local population in Hokkaido. Distinct distribution of the loss-of-function Hd5 revealed that this mutation event of the 19-bp deletion occurred in a local landrace Bouzu and that this mutation may have been selected as an early-heading variety in rice breeding programs in Hokkaido in the early 1900s. The loss-of-function Hd5 was then introduced into the rice variety Fanny from France and contributed to its extremely early heading under the presence of functional Ghd7. These results demonstrated that Hd5 plays roles not only in generating early heading in variations of heading date among a local population in Hokkaido, but also in extremely early heading for adaptation to northern limits of rice cultivation
Dorian Q Fuller's insight:
Although the particular heading date mutation this paper focuses on it perhaps just over 100 years old, as an adaptation to growing rice in Hokkaido, it illustrated the more general principle the northward spread of rice required geneitc adaptations to shorter growing seasons. (See also the DTH2 paper scooped a few weeks ago).
This study offers evidence of the robustness of farmer rice varieties (Oryza glaberrima and O. sativa) in West Africa. Our experiments in five West African countries showed that farmer varieties were tolerant of sub-optimal conditions, but employed a range of strategies to cope with stress. Varieties belonging to the species Oryza glaberrima – solely the product of farmer agency – were the most successful in adapting to a range of adverse conditions. Some of the farmer selections from within the indica and japonica subspecies of O. sativa also performed well in a range of conditions, but other farmer selections from within these two subspecies were mainly limited to more specific niches. The results contradict the rather common belief that farmer varieties are only of local value. Farmer varieties should be considered by breeding programmes and used (alongside improved varieties) in dissemination projects for rural food security.
29 April 2014. Cover of PNAS. The issue with the special feature on the "Modern View of Domestication". Cover image: Pictured are the Gamo-Gofa highlands of southern Ethiopia, a traditional agricultural landscape dotted with domesticated plants and animals such as hybrid cattle. Domesticated plants of diverse geographical origins include maize, sorghum, barley, Ethiopian banana, palm kale, and castor oil plant. The Modern View of Domestication Special Feature, appearing in this issue, presents recent genetic and archaeological evidence regarding the origin and spread of domesticated plants and animals, and addresses questions including those concerning the speed and intentionality of early domestication. See the Introduction to the Special Feature by Greger Larson et al. on pages 6139–6146. Image courtesy of Dorian Fuller.
Agriculture was a transformative development in the history of human societies and natural environments and drove the evolution of new domesticated species. Crop plants are the predominant domesticated species in most agricultural systems and are an essential component in all the food production systems that underpinned the development of urban societies. Archaeological plant remains provide a range of insights into the processes by which plants were domesticated in different parts of the world. The present paper provides a unique synthesis of evidence, including quantitative evidence on the trajectory and rate of domestication in seed crops and patterns in the development of tropical vegetatively propagated crops
Dorian Q Fuller's insight:
This paper includes the most upto date data on archaeologically documented domestication traits in rice, include non-shattering spikelet bases from China, and grain size change in both China and India.
In this study, using a series of BC5F4 nearly isogenic lines (NILs) that were derived from a cross between the Korean japonica cultivar Hwayeongbyeo and Oryza rufipogon, we demonstrated that 2 QTLs, qSPP5 for spikelets per panicle (SPP) and qTGW5 for grain weight (TGW), are tightly linked on chromosome 5. Alleles from the O. rufipogon parent increased the SPP and decreased TGW in the Hwayeongbyeo background. qSPP5 was located within a 803-kb interval between the simple sequence repeat (SSR) markers INDEL3 and RM18076. Based on the map position, qTGW5 seemed to be the same gene as qSW5, which controls grain morphology. The additive effect of theO. rufipogon allele at qSPP5 was 10–15 SPP, and 33.0% of the phenotypic variance could be explained by the segregation of the SSR marker RM18058. Yield trials with BC5F4 NILs showed that lines that contained a homozygous O. rufipogon introgression at the qSPP5 region out-yielded sibling NILs that contained Hwayeongbyeo DNA by 15.3% and out-yielded the Hwayeongbyeo parent by 7.3%.
Based on the finding that the O. rufipogon allele for the SPP was beneficial in the japonica andindica cultivar backgrounds, the qSPP5 allele could be valuable for improving rice yields. In addition, the NIL populations and molecular markers are useful for cloning qSPP5.
Dorian Q Fuller's insight:
So linked alleles for grain number and grain size! This really does mean that unintentional selection for larger grain, parts of the domestication syndrome, would lead to early gains for cultivators potentially offsetting the added labour of cultivation over foraging. This fits the model on entanglement put forward in World Archaeology 42(1) (http://dx.doi.org/10.1080/00438240903429680) but even more dramatically so. It is also worth noting that this may be a specifically japonica rice domestication entanglement and one that was no readily available in early proto-indica, but was introgressed from japonica.
Believe it or not, rice, our staple crop, was not introduced to our island by Aryan migrants from Eastern India around the 5th century BC as had been previously supposed. Rather its cultivation seems to go back to pre-historic times, in all probability to Sri Lanka’s Stone Age
Dorian Q Fuller's insight:
So the claim is made that there was a period of indigenous rice cultivation in the early Holocene of Sri Lanka, that was in the middle Holocene. Not implausible, perhaps, but certainly not proven. (1) Sri Lanka has a rich range of wild rices, both progenitor and non-progenitor species; (2) the evidence of phytoliths cannot easily or relaibly differentiate morphologixall wild versus domesticated rices, although phytoliths assemablges can be useful for determining ecology and this inferred cultivated versus wild ecologies (as we are finding in early China), but such evidence has (not yet) be made available in this case. As happens all too often journalistic headlines trump real science, which is a pity, but core sequences of pollen and phytoliths from Sri Lanka will indeed prove to be important for reconsturcting the prehistory of the island. So too will be rejecting predjudices, expressed by this journalist, that hunter-gatherers (like Veddahs) should be assumed to be "stupid" (and by implication only farmers are "intelligent"). All humans are intelligent have expressed this in many different ways-- adapting to the tropical rainforests through microlithihc tools and hunting of arboreal game some 40,000 years ago-- which is evidence in Sri Lanka-- is one means by which they have done so.(see, e.g. http://www.sciencedirect.com/science/article/pii/S0047248411000881 )
Domestication is a good model for the study of evolutionary processes because of the recent evolution of crop species (<12,000 years ago), the key role of selection in their origins, and good archaeological and historical data on their spread and diversification. Recent studies, such as quantitative trait locus mapping, genome-wide association studies and whole-genome resequencing studies, have identified genes that are associated with the initial domestication and subsequent diversification of crops. Together, these studies reveal the functions of genes that are involved in the evolution of crops that are under domestication, the types of mutations that occur during this process and the parallelism of mutations that occur in the same pathways and proteins, as well as the selective forces that are acting on these mutations and that are associated with geographical adaptation of crop species.
Quantitative description of changes in the distribution of paddy rice cultivation in response to recent climate change provides a reference for rice cultivation patterns and formulation of countermeasures to cope with future climate change in China. This study analyzes the dynamics of decadal changes in distribution of double-cropping rice in China during 1961–2010 in relation to climate change based on the maximum entropy method. Decadal changes in the double-cropping rice cultivation area and climatic suitability in China were apparent. The total area of climatically suitable regions was highest in the 1960s, and subsequently showed an increasing trend at first and then a decreasing trend from the 1970s to 2000s. However, the low climatic suitability area decreased, which implied that the moderate and high climatic suitability areas increased. Among the latter, the high climatic suitability area showed the highest increase in extent to 4.4 times that of the 1990s and four times that of the 1960s. The areas of double-cropping rice cultivation most sensitive to climate change are mainly located in central Jiangsu, central Anhui, the eastern Sichuan Basin, southern Henan and central Guizhou. Transformation of areas between low and moderate climatic suitability was observed in northern Zhejiang, southern Anhui and Hubei, and northern Guangxi. Transformation of areas between moderate and high climatic suitability was observed in central Jiangxi and Leizhou Peninsula. The northern boundary of double-cropping rice cultivation in China shifted southwards and contracted eastwards in the 1970s, and extended northwards in the 1980s. However, the northern boundary did not shift northwards in response to climate warming in the 2000s.
Yield, water productivity and weed-inflicted Relative Yield Losses (RYL) under Recommended Management Practices (RMP) were compared with the System of Rice Intensification (SRI) under double-cropping for two seasons and at two locations in the Senegal River Valley. Seven genotypes from Oryza sativa and Oryza glaberrima species and their interspecific crosses, were grown under weed-free conditions and in competition with weeds. Weed-free grain yields in SRI were never significantly different than those obtained with RMP. An average of 27% (range 18–46%) less water was applied to SRI than required for continuous flooding in RMP, resulting in consistently higher water productivity with SRI. However, when subjected to weed competition, mean SRI yields were significantly lower than RMP in three of four experimental iterations (an average of 28% less). Across experiments, weed-inflicted RYL was greater in SRI than RMP in 81% of observed cases. Weeds reduced the water productivity enhancing benefits of SRI by an average of 38% compared to weed-free treatments, resulting in significantly lower water productivity with SRI in three of four experiments. Rice genotypes Jaya and Sahel-202 were identified as relatively weed-competitive under each crop management system, however both have intermediate-length cycles and required more irrigation than shorter-duration genotypes. When weeds are carefully controlled, good yields and significant water savings can be achieved with SRI. However, this specific requirement of careful weed control might be difficult to meet by farmers coping with high weed infestations or with limited access to tools, inputs or labor to address them. Weed-competitive genotypes could help reduce weed-inflicted yield losses associated with SRI and other water-saving rice production systems, though future breeding efforts should address the trade-offs between weed competitive traits, water productivity and crop duration to meet the needs of farmers practicing double rice cropping.
Tandem and segmental duplications significantly contribute to gene family expansion and genome evolution. Genome-wide identification of tandem and segmental genes has been analyzed before in several plant genomes. However, comparative studies in functional bias, expression divergence and their roles in species domestication are still lacking. We have carried out a genome-wide identification and comparative analysis of tandem and segmental genes in the rice genome. A total of 3,646 and 3,633 pairs of tandem and segmental genes, respectively, were identified in the genome. They made up around 30% of total annotated rice genes (excluding transposon-coding genes). Both tandem and segmental duplicates showed different physical locations and exhibited a biased subset of functions. These two types of duplicated genes were also under different functional constrains as shown by nonsynonymous substitutions per site (Ka) and synonymous substitutions per site (Ks) analysis. They are also differently regulated depending on the tissues and abiotic and biotic stresses based on transcriptomics data. The expression divergence might be related to promoter differentiation and DNA methylation status after tandem or segmental duplications. Both tandem and segmental duplications differ in their contribution to genetic novelty but evidence suggests that they play their role in species domestication and genome evolution
Dorian Q Fuller's insight:
Shows there are quite alot of duplicated genes in the rice genome. Unfortunately, the number that were involved in the domestication process remains speculative-- and needs to be investigated!
Seed development, especially the relevant regulatory mechanism and genetic network are of fundamental scientific interest. Seed development consists of the development of embryo and endosperm; and endosperm development of rice (model species of monocots) is closely related to grain yield and quality. Recent genetic studies, together with other approaches, including transcriptome and proteomics analysis, high-throughput sequencing (RNA-seq, ChIP-seq), revealed the crucial roles of genetic and epigenetic controls in rice endosperm development. Here we summarize and update the genetic networks involved in the regulation of endosperm initiation, cell cycle regulation, aleurone layer specification, starch synthesis, storage protein accumulation and endosperm size, and the interactions between embryo and endosperm.
Dorian Q Fuller's insight:
Looks like a very useful review of the various genes affecting rice grain development, from waxy starch to grain width. Many of these could be selected during various stages in domestication history.
The start of the period of large-scale human effects on this planet (the Anthropocene) is debated. The industrial view holds that most significant impacts have occurred since the early industrial era (1850), whereas the early-anthropogenic view recognizes large impacts thousands of years earlier. This review focuses on three indices of global-scale human influence: forest clearance (and related land use), emissions of greenhouse gases (CO2 and CH4), and effects on global temperature. Because reliable, systematic land-use surveys are rare prior to 1950, most reconstructions for early-industrial centuries and prior millennia are hind casts that assume humans have used roughly the same amount of land per person for 7,000 years. But this assumption is incorrect. Historical data and new archeological databases reveal much greater per-capita land use in preindustrial than in recent centuries. This early forest clearance caused much greater preindustrial greenhousegas emissions and global temperature changes than those proposed within the industrial paradigm.
Dorian Q Fuller's insight:
An excellent updated review on the early anthropogenic greenhouse gas hypothesis by William Ruddiman. nicekly illustrated, including some nice reuse of the maps and data in our Holocene paper on Rice, cows and methane (Fuller & al 2011)
Microsatellites were able to retrieve the well-established classification into Indica (isozyme group 1), Japonica (group 6, comprising temperate and tropical forms) and specific groups from the Himalayan foothills including some Aus varieties (group 2) and some aromatic varieties (group 5). They revealed a new cluster of accessions close to, but distinct from, non-Myanmar varieties in group 5. With reference to earlier terminology, we propose to distinguish a group “5A” including group 5 varieties from the Indian subcontinent (South and West Asia) and a group “5B” including most group 5 varieties from Myanmar. In Myanmar varieties, aroma was distributed in group 1 (Indica) and in group 5B. New BADH2 variants were found. Some accessions carried a 43 bp deletion in the 3’ UTR that was not completely associated with aroma. Other accessions, all of group 5B, displayed a particularBADH2 allele with a 3 bp insertion and 100% association with aroma. With the new group and the new alleles found in Myanmar varieties, our study shows that the Himalayan foothills contain series of non-Indica and non-Japonica varietal types with novel variations for useful traits.
Reduction in seed shattering was an important phenotypic change during cereal domestication. Here we show that a simple morphological change in rice panicle shape, controlled by the SPR3 locus, has a large impact on seed-shedding and pollinating behaviors. In the wild genetic background of rice, we found that plants with a cultivated-like type of closed panicle had significantly reduced seed shedding through seed retention. In addition, the long awns in closed panicles disturbed the free exposure of anthers and stigmas on the flowering spikelets, resulting in a significant reduction of the outcrossing rate. We localized the SPR3 locus to a 9.3-kb genomic region, and our complementation tests suggest that this region regulates the liguleless gene (OsLG1). Sequencing analysis identified reduced nucleotide diversity and a selective sweep at theSPR3 locus in cultivated rice. Our results suggest that a closed panicle was a selected trait during rice domestication.
Dorian Q Fuller's insight:
This is further important work from the Kobe University rice research group (Ishii, Ishikawa, and colleagues) which derives from careful experimental growing on wild rice and breeding of crop traits in wild rices. A few years ago they showed that sh4 alone was not apparently an effective mutation for non-shattering, as normally inferred, but required additional interacting mutations. They have identified a key trait (if not the key trait), SPR3, which delays shattering, and together with sh4 essentially leads to the key domestication trait of non-shattering. Of particular interest it is has the side effect of decreasing cross pollination, and thus pushing rice towards selfing, another key change with domestication. The main feaure of SPR3 seems to be towards a closed (and less branching) panicle, which we would expect to have the effect of making it easier to gather a larger proportion of grains when harvesting using hunter-gatherer methods like basket beating. Ethnographically wild rice gathering (including of Zizania amongst the Ojibwa) often features tieing panicles into a knot after flowering when grains are green so as to catch early shattering grains. Essentially this mutation achieves a similar end and we might therefore see this as likely quite early in the domestication process. I suspect this goes some way towards helping explain how rice domesticiation worked in the absence of sickles (which are 3rd Millennium BC in the Yangtze), a clear contrast from wheat and barley. It is also worth noting that long awns play a role in retaining mature grains, which goes some way to explain why selection for awnlessness is so clearly an incomplete and post-domestication development.
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