Juan Yan

Variability and adaptability of Miscanthus species evaluated for energy crop domestication

A growing body of evidence indicates that second‐generation energy crops can play an important role in the development of renewable energy and the mitigation of climate change. However, dedicated energy crops have yet to be domesticated in order to fully realize their productive potential under unfavorable soil and climatic conditions. To explore the possibility of domesticating Miscanthus crops in northern China where marginal and degraded land is abundant, we conducted common garden experiments at multiple locations to evaluate variation and adaptation of three Miscanthus species that are likely to serve as the wild progenitors of the energy crops. A total of 93 populations of Miscanthus sinensis, Miscanthus sacchariflorus, and Miscanthus lutarioriparius were collected across their natural distributional ranges in China and grown in three locations that represent temperate grassland with cold winter, the semiarid Loess Plateau, and relatively warm and wet central China. Evaluated with growth traits such as plant height, tiller number, tiller diameter, and flowering time, the Miscanthus species showed high levels of genetic variation within and between species. There were significant site × population interactions for almost all traits of M. sacchariflorus and M. sinensis, but not M. lutarioriparius. The northern populations of M. sacchariflorus had the highest establishment rates at the most northern site owing to their strong cold tolerance. An endemic species in central China, M. lutarioriparius, produced not only the highest biomass of the three species but also higher biomass at the Loess Plateau than the southern site near its native habitats. These results demonstrated that the wild species harbored a high level of genetic variation underlying traits important for crop establishment and production at sites that are colder and drier than their native habitats. The natural variation and adaptive plasticity found in the Miscanthus species indicated that they could provide valuable resources for the development of second‐generation energy crops.

Yield potential of Miscanthus energy crops in the Loess Plateau of China

Growing second‐generation energy crops on marginal land is conceptualized as one of the primary means of future bioenergy development. However, the extent to which marginal land can support energy crop production remains unclear. The Loess Plateau of China, one of the most seriously eroded regions of the world, is particularly rich in marginal land. On the basis of the previous field experiment of planting Miscanthus species in Qingyang of the Gansu Province, herein, we estimated the yield potential of Miscanthus lutarioriparius, the species with the highest biomass, across the Loess Plateau. On the basis of the radiation model previously developed from Miscanthus field trials, annual precipitation was introduced as an additional variable for yield estimate in the semiarid and semihumid regions of the Loess Plateau. Of 62 million hectares (Mha) of the Loess Plateau, our model estimated that 48.7 Mha can potentially support Miscanthus growth, with the average yield of 17.8 t ha−1 yr−1. After excluding high‐quality cropland and pasture and land suitable for afforestation, a total of 33.3 Mha of presumably marginal land were left available for producing the energy crop at the average yield of 16.8 t ha−1 yr−1 and the total annual yield of 0.56 billion tons. The analysis of environmental factors indicated that erosion, aridity, and field steepness were the primary contributors to the poor quality of the marginal land. The change of land uses from traditional agriculture to energy crop production may prevent further erosion and land degradation and consequently establish a sustainable economy for the region.

Population genetic structure of two Medicago species shaped by distinct life form, mating system and seed dispersal.

BACKGROUND AND AIMS Life form, mating system and seed dispersal are important adaptive traits of plants. In the first effort to characterize in detail the population genetic structure and dynamics of wild Medicago species in China, a population genetic study of two closely related Medicago species, M. lupulina and M. ruthenica, that are distinct in these traits, are reported. These species are valuable germplasm resources for the improvement of Medicago forage crops but are under threat of habitat destruction. METHODS Three hundred and twenty-eight individuals from 16 populations of the annual species, M. lupulina, and 447 individuals from 15 populations of the perennial species, M. ruthenica, were studied using 15 and 17 microsatellite loci, respectively. Conventional and Bayesian-clustering analyses were utilized to estimate population genetic structure, mating system and gene flow. KEY RESULTS Genetic diversity of M. lupulina (mean H(E)=0.246) was lower than that of M. ruthenica (mean H(E)=0.677). Populations of M. lupulina were more highly differentiated (F(ST)=0.535) than those of M. ruthenica (F(ST)=0.130). For M. lupulina, 55.5% of the genetic variation was partitioned among populations, whereas 76.6% of the variation existed within populations of M. ruthenica. Based on the genetic data, the selfing rates of M. lupulina and M. ruthenica were estimated at 95.8% and 29.5%, respectively. The genetic differentiation among populations of both species was positively correlated with geographical distance. CONCLUSIONS The mating system differentiation estimated from the genetic data is consistent with floral morphology and observed pollinator visitation. There was a much higher historical gene flow in M. ruthenica than in M. lupulina, despite more effective seed dispersal mechanisms in M. lupulina. The population genetic structure and geographical distribution of the two Medicago species have been shaped by life form, mating systems and seed dispersal mechanisms.

Carbon sequestration by Miscanthus energy crops plantations in a broad range semi-arid marginal land in China

Carbon sequestration is an essential ecosystem service that second-generation energy crops can provide. To evaluate the ability of carbon sequestration of Miscanthus energy crops in the Loess Plateau of China, the yield and soil organic carbon (SOC) changes were measured for three Miscanthus species in the experimental field in Qingyang of the Gansu Province (QG). With the highest yield of the three species, Miscanthus lutarioriparius contributed to the largest increase of SOC, 0.57 t ha(-1)yr(-1), comparing to the field left unplanted. Through modeling M. lutarioriparius yield across the Loess Plateau, an average increase of SOC was estimated at 0.46 t ha(-1)yr(-1) for the entire region. Based on the measurements of SOC mineralization under various temperatures and moistures for soil samples taken from QG, a model was developed for estimating SOC mineralization rates across the Loess Plateau and resulted in an average of 1.11 t ha(-1)yr(-1). Combining the estimates from these models, the average of net carbon sequestration was calculated at a rate of 9.13 t ha(-1)yr(-1) in the Loess Plateau. These results suggested that the domestication and production of M. lutarioriparius hold a great potential for carbon sequestration and soil restoration in this heavily eroded region.

High photosynthetic rate and water use efficiency of Miscanthus lutarioriparius characterize an energy crop in the semiarid temperate region

The development of second‐generation energy crops on marginal land relies on the identification of plants with suitable physiological properties. In this study, we measured and compared leaf photosynthesis and water use efficiency of 22 populations from three Miscanthus species, M. lutarioriparius, M. sacchariflorus, and M. sinensis, planted in two experimental fields located in Qingyang of the Gansu Province (QG) and Jiangxia of the Hubei Province (JH) in China. QG is located in the Loess Plateau, one of the worlds most seriously eroded regions particularly abundant in semiarid marginal land. At both locations, M. lutarioriparius produced the highest biomass and had the highest photosynthetic rates (A), with the growing‐season average of A reaching nearly 20 μmol m−2 s−1. Native to JH, M. lutarioriparius maintained a relatively high photosynthetic rate into the late growing stage in QG, for example, 15 μmol m−2 s−1 at temperature as low as 11.6 °C in October. All three species had higher water use efficiency (WUE) in semiarid QG than in warmer and wetter JH. In the late growing stage of M. lutarioriparius, instantaneous WUE (A/E) of the species nearly tripled in QG comparing to JH. Being able to maintain remarkably high photosynthetic rates when transplanted to a colder and drier location, these M. lutarioriparius populations serve as suitable wild progenitors for energy crop domestication in the Loess Plateau and other areas with the similar climates.

Transcriptome-wide characterization of candidate genes for improving the water use efficiency of energy crops grown on semiarid land

Highlight A matrix correlation analysis between transcriptome-wide expression levels and water use efficiency of Miscanthus lutarioriparius identified candidate genes facilitating adaptation of the energy crop to semiarid marginal land.

Genetic variation and bidirectional gene flow in the riparian plant Miscanthus lutarioriparius, across its endemic range: implications for adaptive potential

Miscanthus lutarioriparius is an endemic species that grows along the middle and lower reaches of the Yangtze River and is a valuable source of germplasm for the development of second‐generation energy crops. The plant that propagates via seeds, stem nodes, and rhizomes shows high phenotypic variation and strong local adaptation. Here, we examined the magnitude and spatial distribution of genetic variation in M. lutarioriparius across its entire distributional range and tested underlying factors that shaped its genetic variation. Population genetic analyses were conducted on 644 individuals from 25 populations using 16 microsatellite markers. M. lutarioriparius exhibited a high level of genetic variation (HE = 0.682–0.786; Ar = 4.74–8.06) and a low differentiation (FST = 0.063; Dest = 0.153). Of the total genetic variation, 10% was attributed to the differences among populations (df = 24, P < 0.0001), whereas 90% was attributed to the differences among individuals (df = 619, P ≤ 0.0001). Genetic diversity did not differ significantly across longitudes and did not increase in the populations growing downstream of the Yangtze River. However, significant associations were found between genetic differentiation and spatial distance. Six genetic discontinuities were identified, which mostly distributed among downstream populations. We conclude that anthropogenic factors and landscape features both contributed to shaping the pattern of gene flow in M. lutarioriparius, including long‐distance bidirectional dispersal. Our results explain the genetic basis of the high degree of adaptability in M. lutarioriparius and identify potential sources of new germplasm for the domestication of this potential second‐generation energy crop.

Population transcriptomics reveals a potentially positive role of expression diversity in adaptation

While it is widely accepted that genetic diversity determines the potential of adaptation, the role that gene expression variation plays in adaptation remains poorly known. Here we show that gene expression diversity could have played a positive role in the adaptation of Miscanthus lutarioriparius. RNA-seq was conducted for 80 individuals of the species, with half planted in the energy crop domestication site and the other half planted in the control site near native habitats. A leaf reference transcriptome consisting of 18,503 high-quality transcripts was obtained using a pipeline developed for de novo assembling with population RNA-seq data. The population structure and genetic diversity of M. lutarioriparius were estimated based on 30,609 genic single nucleotide polymorphisms. Population expression (Ep ) and expression diversity (Ed ) were defined to measure the average level and the magnitude of variation of a gene expression in the population, respectively. It was found that expression diversity increased while genetic diversity decreased after the species was transplanted from the native habitats to the harsh domestication site, especially for genes involved in abiotic stress resistance, histone methylation, and biomass synthesis under water limitation. The increased expression diversity could have enriched phenotypic variation directly subject to selections in the new environment.

Population transcriptomics uncovers the regulation of gene expression variation in adaptation to changing environment

Expression variation plays an important role in plant adaptation, but little is known about the factors impacting the expression variation when population adapts to changing environment. We used RNA-seq data from 80 individuals in 14 Miscanthus lutarioriparius populations, which were transplanted into a harsh environment from native habitat, to investigate the expression level, expression diversity and genetic diversity for genes expressed in both environments. The expression level of genes with lower expression level or without SNP tended to be more changeable in new environment, which suggested highly expressed genes experienced stronger purifying selection than those at lower level. Low proportion of genes with population effect confirmed the weak population structure and frequent gene flow in these populations. Meanwhile, the number of genes with environment effect was the most frequent compared with that with population effect. Our results showed that environment and genetic diversity were the main factors determining gene expression variation in population. This study could facilitate understanding the mechanisms of global gene expression variation when plant population adapts to changing environment.

Systematic comparison of lncRNAs with protein coding mRNAs in population expression and their response to environmental change

BackgroundLong non-coding RNA (lncRNA) is a class of non-coding RNA with important regulatory roles in biological process of organisms. The systematic comparison of lncRNAs with protein coding mRNAs in population expression and their response to environmental change are still poorly understood. Here we identified 17,610 lncRNAs and calculated their expression levels based on RNA-seq of 80 individuals of Miscanthus lutarioriparius from two environments, the nearly native habitats and transplanted field, respectively.ResultsLncRNAs had significantly higher expression diversity and lower expression frequency in population than protein coding mRNAs in both environments, which suggested that lncRNAs may experience more relaxed selection or divergent evolution in population compared with protein coding RNAs. In addition, the increase of expression diversity for lncRNAs was always significantly higher and the magnitude of fold change of expression in new stress environment was significantly larger than protein-coding mRNAs. These results suggested that lncRNAs may be more sensitive to environmental change than protein-coding mRNAs. Analysis of environment-robust and environment-specific lncRNA-mRNA co-expression network between two environments revealed the characterization of lncRNAs in response to environmental change. Furthermore, candidate lncRNAs contributing to water use efficiency (WUE) identified based on the WUE-lncRNA-mRNA co-expression network suggested the roles of lncRNAs in response to environmental change.ConclusionOur study provided a comprehensive understanding of expression characterization of lncRNAs in population for M. lutarioriparius under field condition, which would be useful to explore the roles of lncRNAs and could accelerate the process of adaptation in new environment for many plants.