Title: Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C 4 grass
Abstract
Photoperiod is a key environmental cue affecting flowering and biomass traits in plants. Key components of the photoperiodic flowering pathway have been identified in many species, but surprisingly few studies have globally examined the diurnal rhythm of gene expression with changes in day length. Using a cost‐effective 3′‐Tag RNA sequencing strategy, we characterize 9,010 photoperiod responsive genes with strict statistical testing across a diurnal time series in the C4perennial grass,Panicum hallii. We show that the vast majority of photoperiod responses are driven by complex interactions between day length and sampling periods. A fine‐scale contrast analysis at each sampling time revealed a detailed picture of the temporal reprogramming ofcis‐regulatory elements and biological processes under short‐ and long‐day conditions. Phase shift analysis reveals quantitative variation among genes with photoperiod‐dependent diurnal patterns. In addition, we identify three photoperiod enriched transcription factor families with key genes involved in photoperiod flowering regulatory networks. Finally, coexpression networks analysis ofGIGANTEAhomolog predicted 1,668 potential coincidence partners, including five well‐known GI‐interacting proteins. Our results not only provide a resource for understanding the mechanisms of photoperiod regulation in perennial grasses but also lay a foundation to increase biomass yield in biofuel crops.
Han, Rongkui; Lavelle, Dean; Truco, Maria José; Michelmore, Richard(
, Theoretical and Applied Genetics)
AbstractKey message
A population of lettuce that segregated for photoperiod sensitivity was planted under long-day and short-day conditions. Genetic mapping revealed two distinct sets of QTLs controlling daylength-independent and photoperiod-sensitive flowering time.
Abstract
The molecular mechanism of flowering time regulation in lettuce is of interest to both geneticists and breeders because of the extensive impact of this trait on agricultural production. Lettuce is a facultative long-day plant which changes in flowering time in response to photoperiod. Variations exist in both flowering time and the degree of photoperiod sensitivity among accessions of wild (Lactuca serriola) and cultivated (L. sativa) lettuce. An F6population of 236 recombinant inbred lines (RILs) was previously developed from a cross between a late-flowering, photoperiod-sensitiveL. serriolaaccession and an early-flowering, photoperiod-insensitiveL. sativaaccession. This population was planted under long-day (LD) and short-day (SD) conditions in a total of four field and screenhouse trials; the developmental phenotype was scored weekly in each trial. Using genotyping-by-sequencing (GBS) data of the RILs, quantitative trait loci (QTL) mapping revealed five flowering time QTLs that together explained more than 20% of the variation in flowering time under LD conditions. Using two independent statistical models to extract the photoperiod sensitivity phenotype from the LD and SD flowering time data, we identified an additional five QTLs that together explained more than 30% of the variation in photoperiod sensitivity in the population. Orthology and sequence analysis of genes within the nine QTLs revealed potential functional equivalents in the lettuce genome to the key regulators of flowering time and photoperiodism,FDandCONSTANS, respectively, in Arabidopsis.
Alfalfa (Medicago sativaL.) is a perennial flowering plant in the legume family that is widely cultivated as a forage crop for its high yield, forage quality and related agricultural and economic benefits. Alfalfa is a photoperiod sensitive long‐day (LD) plant that can accomplish its vegetative and reproductive phases in a short period of time. However, rapid flowering can compromise forage biomass yield and quality. Here, we attempted to delay flowering in alfalfa using multiplex CRISPR/Cas9‐mediated mutagenesis ofFLOWERING LOCUS Ta1(MsFTa1), a key floral integrator and activator gene. Four guide RNAs (gRNAs) were designed and clustered in a polycistronic tRNA–gRNA system and introduced into alfalfa byAgrobacterium‐mediated transformation. Ninety‐six putative mutant lines were identified by gene sequencing and characterized for delayed flowering time and related desirable agronomic traits. Phenotype assessment of flowering time under LD conditions identified 22 independent mutant lines with delayed flowering compared to the control. Six independentMsfta1lines containing mutations in all four copies ofMsFTa1accumulated significantly higher forage biomass yield, with increases of up to 78% in fresh weight and 76% in dry weight compared to controls. Depending on the harvesting schemes, many of these lines also had reduced lignin, acid detergent fibre (ADF) and neutral detergent fibre (NDF) content and significantly higher crude protein (CP) and mineral contents compared to control plants, especially in the stems. These CRISPR/Cas9‐editedMsfta1mutants could be introduced in alfalfa breeding programmes to generate elite transgene‐free alfalfa cultivars with improved forage biomass yield and quality.
Conservative flowering behaviours, such as flowering during long days in summer or late flowering at a high leaf number, are often proposed to protect against variable winter and spring temperatures which lead to frost damage if premature flowering occurs. Yet, due the many factors in natural environments relative to the number of individuals compared, assessing which climate characteristics drive these flowering traits has been difficult. We applied a multidisciplinary approach to 10 winter‐annualArabidopsis thalianapopulations from a wide climactic gradient in Norway. We used a variable reduction strategy to assess which of 100 climate descriptors from their home sites correlated most to their flowering behaviours when tested for responsiveness to photoperiod after saturation of vernalization; then, assessed sequence variation of 19 known environmental‐response flowering genes. Photoperiod responsiveness inversely correlated with interannual variation in timing of growing season onset. Time to flowering appeared driven by growing season length, curtailed by cold fall temperatures. The distribution ofFLM, TFL2 andHOS1haplotypes, genes involved in ambient temperature response, correlated with growing‐season climate. We show that long‐day responsiveness and late flowering may be driven not by risk of spring frosts, but by growing season temperature and length, perhaps to opportunistically maximize growth.
Plants respond to abiotic stress through a variety of physiological, biochemical, and transcriptional mechanisms. Many genes exhibit altered levels of expression in response to abiotic stress, which requires concerted action of bothcis‐andtrans‐regulatory features. In order to study the variability in transcriptome response to abiotic stress,RNAsequencing was performed using 14‐day‐old maize seedlings of inbreds B73, Mo17, Oh43,PH207 and B37 under control, cold and heat conditions. Large numbers of genes that responded differentially to stress between parental inbred lines were identified.RNAsequencing was also performed on similar tissues of theF1hybrids produced by crossing B73 and each of the three other inbred lines. By evaluating allele‐specific transcript abundance in theF1hybrids, we were able to measure the abundance ofcis‐andtrans‐regulatory variation between genotypes for both steady‐state and stress‐responsive expression differences. Although examples oftrans‐regulatory variation were observed,cis‐regulatory variation was more common for both steady‐state and stress‐responsive expression differences. The genes withcis‐allelic variation for response to cold or heat stress provided an opportunity to study the basis for regulatory diversity.
Wu, Faqiang; Sedivy, Eric J.; Price, William Brian; Haider, Waseem; Hanzawa, Yoshie(
, The Plant Journal)
Summary
To clarify the molecular bases of flowering time evolution in crop domestication, here we investigate the evolutionary fates of a set of four recently duplicated genes in soybean:FT2a,FT2b,FT2candFT2dthat are homologues of the floral inducerFLOWERING LOCUST(FT). WhileFT2amaintained the flowering inducer function, other genes went through contrasting evolutionary paths.FT2bevolved attenuated expression potentially associated with a transposon insertion in the upstream intergenic region, whileFT2candFT2dobtained a transposon insertion and structural rearrangement, respectively. In contrast toFT2bandFT2dwhose mutational events occurred before the separation ofG. maxandG. soja, the evolution ofFT2cis aG. maxlineage specific event. TheFT2callele carrying a transposon insertion is nearly fixed in soybean landraces and differentiates domesticated soybean from wild soybean, indicating that this allele spread at the early stage of soybean domestication. The domesticated allele causes later flowering than the wild allele under short day and exhibits a signature of selection. These findings suggest thatFT2cmay have underpinned the evolution of photoperiodic flowering regulation in soybean domestication and highlight the evolutionary dynamics of this agronomically important gene family.
Weng, Xiaoyu, Lovell, John T., Schwartz, Scott L., Cheng, Changde, Haque, Taslima, Zhang, Li, Razzaque, Samsad, and Juenger, Thomas E. Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C 4 grass. Plant, Cell & Environment 42.7 Web. doi:10.1111/pce.13546.
Weng, Xiaoyu, Lovell, John T., Schwartz, Scott L., Cheng, Changde, Haque, Taslima, Zhang, Li, Razzaque, Samsad, & Juenger, Thomas E. Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C 4 grass. Plant, Cell & Environment, 42 (7). https://doi.org/10.1111/pce.13546
Weng, Xiaoyu, Lovell, John T., Schwartz, Scott L., Cheng, Changde, Haque, Taslima, Zhang, Li, Razzaque, Samsad, and Juenger, Thomas E.
"Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C 4 grass". Plant, Cell & Environment 42 (7). Country unknown/Code not available: Wiley-Blackwell. https://doi.org/10.1111/pce.13546.https://par.nsf.gov/biblio/10456781.
@article{osti_10456781,
place = {Country unknown/Code not available},
title = {Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C 4 grass},
url = {https://par.nsf.gov/biblio/10456781},
DOI = {10.1111/pce.13546},
abstractNote = {Abstract Photoperiod is a key environmental cue affecting flowering and biomass traits in plants. Key components of the photoperiodic flowering pathway have been identified in many species, but surprisingly few studies have globally examined the diurnal rhythm of gene expression with changes in day length. Using a cost‐effective 3′‐Tag RNA sequencing strategy, we characterize 9,010 photoperiod responsive genes with strict statistical testing across a diurnal time series in the C4perennial grass,Panicum hallii. We show that the vast majority of photoperiod responses are driven by complex interactions between day length and sampling periods. A fine‐scale contrast analysis at each sampling time revealed a detailed picture of the temporal reprogramming ofcis‐regulatory elements and biological processes under short‐ and long‐day conditions. Phase shift analysis reveals quantitative variation among genes with photoperiod‐dependent diurnal patterns. In addition, we identify three photoperiod enriched transcription factor families with key genes involved in photoperiod flowering regulatory networks. Finally, coexpression networks analysis ofGIGANTEAhomolog predicted 1,668 potential coincidence partners, including five well‐known GI‐interacting proteins. Our results not only provide a resource for understanding the mechanisms of photoperiod regulation in perennial grasses but also lay a foundation to increase biomass yield in biofuel crops.},
journal = {Plant, Cell & Environment},
volume = {42},
number = {7},
publisher = {Wiley-Blackwell},
author = {Weng, Xiaoyu and Lovell, John T. and Schwartz, Scott L. and Cheng, Changde and Haque, Taslima and Zhang, Li and Razzaque, Samsad and Juenger, Thomas E.},
}
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