Caiyun Zhu

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.

Transcriptomic characterization of candidate genes responsive to salt tolerance of Miscanthus energy crops

Given the growing need for biofuel production but the lack of suitable land for producing biomass feedstock, development of stress‐tolerant energy crops will be increasingly important. We used comparative transcriptomics to reveal differential responses to long‐term salt stress among five populations of Miscanthus lutarioriparius grown in the natural habitats and salinity experimental site. A total of 59 genes were found to be potentially responsive to the high‐salinity conditions shared by the five populations, including those involved in detoxification, plant defense, photosynthesis, and signal transduction. Of these genes, about 70% were related to abiotic stress response. Among five populations, the most contrasting performance between relatively high survival rates and the relatively weak growing traits was in accordance with the down‐regulation of genes involved in growth and up‐regulation of genes related to plant stress tolerance in one of the populations. These results might reveal a potential tolerance‐productivity trade‐off, where resources were allocated from growth to stress resistance. The comparative transcriptomics of different populations among different environments will provide a basis for breeding and domestication of energy crops.

The Coordination of Gene Expression within Photosynthesis Pathway for Acclimation of C4 Energy Crop Miscanthus lutarioriparius

As a promising candidate for the second-generation C4 energy crop, Miscanthus lutarioriparius has well acclimated to the water-limited and high-light Loess Plateau in China by improving photosynthesis rate and water use efficiency (WUE) compared to its native habitat along Yangtze River. Photosynthetic genes were demonstrated as one major category of the candidate genes underlying the physiological superiority. To further study how photosynthetic genes interact to improve the acclimation potential of M. lutarioriparius, population expression patterns within photosynthesis pathway were explored between one mild environment and one harsh environment. We found that 108 transcripts in assembled transcriptome of M. lutarioriparius were highly similar to genes in three Kyoto Encyclopedia of Genes and Genomes (KEGG) photosynthesis pathways of sorghum and maize. Phylogenetic analyses using sorghum, maize, rice, and Arabidopsis genes of dark reaction identified 23 orthologs and 30 paralogs of M. lutarioriparius photosynthetic genes. These genes were also clustered into two kinds of expression pattern. 87% of transcripts in dark reaction were up-regulated and all 14 chloroplast-encoded transcripts in light reaction increased degradation in the harsh environment compared to the mild environment. Moreover, 80.8% of photosynthetic transcripts were coordinated at transcription level under the two environments. Interestingly, LHCI and PSI were significantly correlated with F-ATPase and C4 cycle. Overall, this study indicates the coordinated expression between cyclic electron transport (consisting of LHCI, PSI, and ATPase) and CO2-concentrating mechanism (C4 cycle) could account for photosynthesis plasticity on M. lutarioriparius acclimation potential.

Haplotypes Phased from Population Transcriptomes Detecting Selection in the Initial Adaptation of to Stressful Environments

A new method based on allele frequency to detect selection is proposed. Haplotypes were inferred from transcriptomes of 80 individuals. In total, 401 and 52 genes were targets of positive and negative selection respectively. Abiotic‐related and photosynthesis‐related genes were enriched in targeted genes.

Population transcriptomic characterization of the genetic and expression variation of a candidate progenitor of Miscanthus energy crops

The use of transcriptome data in the study of the population genetics of a species can capture faint signals of both genetic variation and expression variation and can provide a broad picture of a species’ genomic response to environmental conditions. In this study, we characterized the genetic and expression diversity of Miscanthus lutarioriparius by comparing more than 16,225 transcripts obtained from 78 individuals, belonging to 10 populations distributed across the species’ entire geographic range. We only observed a low level of nucleotide diversity (π = 0.000434) among the transcriptome data of these populations, which is consistent with highly conserved sequences of functional elements and protein‐coding genes captured with this method. Tests of population divergence using the transcriptome data were consistent with previous microsatellite data but proved to be more sensitive, particularly if gene expression variation was considered as well. For example, the analysis of expression data showed that genes involved in photosynthetic processes and responses to temperature or reactive oxygen species stimuli were significantly enriched in certain populations. This differential gene expression was primarily observed among populations and not within populations. Interestingly, nucleotide diversity was significantly negatively correlated with expression diversity within populations, while this correlation was positive among populations. This suggests that genetic and expression variation play separate roles in adaptation and population persistence. Combining analyses of genetic and gene expression variation represents a promising approach for studying the population genetics of wild species and may uncover both adaptive and nonadaptive processes.