The ratio of plant carbon gain to water use, known as water use efficiency (WUE), has long been recognized as a key constraint on crop production and an important target for crop improvement. WUE is a physiologically and genetically complex trait that can be defined at a range of scales. Many component traits directly influence WUE, including photosynthesis, stomatal and mesophyll conductances, and canopy structure. Interactions of carbon and water relations with diverse aspects of the environment and crop development also modulate WUE. As a consequence, enhancing WUE by breeding or biotechnology has proven challenging but not impossible. This review aims to synthesize new knowledge of WUE arising from advances in phenotyping, modeling, physiology, genetics, and molecular biology in the context of classical theoretical principles. In addition, we discuss how rising atmospheric CO2 concentration has created and will continue to create opportunities for enhancing WUE by modifying the trade-off between photosynthesis and transpiration.
Sorghum (Sorghum bicolor L.) is a major food cereal for millions of people worldwide. The sorghum genome, like other species, accumulates deleterious mutations, likely impacting its fitness. The lack of recombination, drift, and the coupling with favorable loci impede the removal of deleterious mutations from the genome by selection. To study how deleterious variants impact phenotypes, we identified putative deleterious mutations among ∼5.5 M segregating variants of 229 diverse biomass sorghum lines. We provide the whole-genome estimate of the deleterious burden in sorghum, showing that ∼33% of nonsynonymous substitutions are putatively deleterious. The pattern of mutation burden varies appreciably among racial groups. Across racial groups, the mutation burden correlated negatively with biomass, plant height, specific leaf area (SLA), and tissue starch content (TSC), suggesting that deleterious burden decreases trait fitness. Putatively deleterious variants explain roughly one-half of the genetic variance. However, there is only moderate improvement in total heritable variance explained for biomass (7.6%) and plant height (average of 3.1% across all stages). There is no advantage in total heritable variance for SLA and TSC. The contribution of putatively deleterious variants to phenotypic diversity therefore appears to be dependent on the genetic architecture of traits. Overall, these results suggest that incorporating putatively deleterious variants into genomic models slightly improves prediction accuracy because of extensive linkage. Knowledge of deleterious variants could be leveraged for sorghum breeding through either genome editing and/or conventional breeding that focuses on the selection of progeny with fewer deleterious alleles.
The ability of plants to acquire and use water is critical in determining life-history traits such as growth, flowering, and allocation of biomass into reproduction. In this context, a combination of functionally linked traits is essential for plants to respond to environmental changes in a coordinated fashion to maximize resource use efficiency. We analyzed different water-use traits in Arabidopsis ecotypes to identify functionally linked traits that determine water use and plant growth performance.Water-use traits measured were (i) leaf-level water-use efficiency (WUE i ) to evaluate the amount of CO 2 fixed relative to water loss per leaf area and (ii) short-term plant water use at the vegetative stage (VWU) as a measure of whole-plant transpiration. Previously observed phenotypic variance in VWU, WUE i and life-history parameters, highlighted C24 as a valuable ecotype that combined drought tolerance, preferential reproductive biomass allocation, high WUE i , and reduced water use. We therefore screened 35 Arabidopsis ecotypes for these parameters, in order to assess whether the phenotypic combinations observed in C24 existed more widely within Arabidopsis ecotypes. All parameters were measured on a short dehydration cycle.A segmented regression analysis was carried out to evaluate the plasticity of the drought response and identified the breakpoint as a reliable measure of drought sensitivity. VWU was largely dependent on rosette area, but importantly the drought sensitivity and plasticity measures were independent of the transpiring leaf surface. A breakpoint at high rSWC indicated a more drought-sensitive plant that closed stomata early during the dehydration cycle and consequently showed stronger plasticity in leaf-level WUE i parameters. None of the sensitivity, plasticity, or water-use measurements were able to predict the overall growth performance; however, there was a general trade-off between vegetative and reproductive biomass. PCA and hierarchical clustering revealed that C24 was unique among the 35 ecotypes in uniting all the beneficial water use and stress tolerance traits, while also maintaining above average plant growth. We propose that a short dehydration cycle, measuring drought sensitivity and VWU is a fast and reliable screen for plant water use and drought response strategies.--
Crop losses caused by plant pathogens are a primary threat to stable food production. Stripe rust (Puccinia striiformis) is a fungal pathogen of cereal crops that causes significant, persistent yield loss. Stripe rust exhibits host species specificity, with lineages that have adapted to infect wheat and barley. While wheat stripe rust and barley stripe rust are commonly restricted to their corresponding hosts, the genes underlying this host specificity remain unknown. Here, we show that three resistance genes, Rps6, Rps7, and Rps8, contribute to immunity in barley to wheat stripe rust. Rps7 cosegregates with barley powdery mildew resistance at the Mla locus. Using transgenic complementation of different Mla alleles, we confirm allele-specific recognition of wheat stripe rust by Mla. Our results show that major resistance genes contribute to the host species specificity of wheat stripe rust on barley and that a shared genetic architecture underlies resistance to the adapted pathogen barley powdery mildew and non-adapted pathogen wheat stripe rust.
Sorghum (Sorghum bicolor) is a model C4 crop made experimentally tractable by extensive genomic and genetic resources. Biomass sorghum is studied as a feedstock for biofuel and forage. Mechanistic modelling suggests that reducing stomatal conductance (gs) could improve sorghum intrinsic water use efficiency (iWUE) and biomass production. Phenotyping to discover genotype-to-phenotype associations remains a bottleneck in understanding the mechanistic basis for natural variation in gs and iWUE. This study addressed multiple methodological limitations. Optical tomography and a machine learning tool were combined to measure stomatal density (SD). This was combined with rapid measurements of leaf photosynthetic gas exchange and specific leaf area (SLA). These traits were the subject of genome-wide association study (GWAS) and transcriptome-wide association study (TWAS) across 869 field-grown biomass sorghum accessions. The ratio of intracellular to ambient CO2 (ci/ca) was genetically correlated with SD, SLA, gs and biomass production. Plasticity in SD and SLA were interrelated with each other and with productivity across wet and dry growing seasons. Moderate-to-high heritability of traits studied across the large mapping population validated associations between DNA sequence variation or RNA transcript abundance and trait variation. 394 unique genes underpinning variation in WUE-related traits are described with higher confidence because they were identified in multiple independent tests. This list was enriched in genes whose Arabidopsis (Arabidopsis thaliana) putative orthologs have functions related to stomatal or leaf development and leaf gas exchange, as well as genes with non-synonymous/missense variants. These advances in methodology and knowledge will facilitate improving C4 crop WUE.
A key target for the improvement of Oryza sativa (rice) is the development of heat-tolerant varieties. This necessitates the development of high-throughput methodologies for the screening of heat tolerance. Progress has been made to this end via visual scoring and chlorophyll fluorescence; however, these approaches demand large infrastructural investments to expose large populations of adult plants to heat stress. To address this bottleneck, we investigated the response of the maximum quantum efficiency of photosystem II (PSII) to rapidly increasing temperatures in excised leaf segments of juvenile rice plants. Segmented models explained the majority of the observed variation in response. Coefficients from these models, i.e. critical temperature (T crit) and the initial response (m 1), were evaluated for their usability for forecasting adult heat tolerance, measured as the vegetative heat tolerance of adult rice plants through visual (stay-green) and chlorophyll fluorescence (ɸPSII) approaches. We detected substantial variation in heat tolerance of a randomly selected set of indica rice varieties. Both T crit and m 1 were associated with measured heat tolerance in adult plants, highlighting their usability as high-throughput proxies. Variation in heat tolerance was associated with daytime respiration but not with photosynthetic capacity, highlighting a role for the non-photorespiratory release of CO 2 in heat tolerance. To date, this represents the first published instance of genetic variation in these key gas-exchange traits being quantified in response to heat stress in a diverse set of rice accessions. These results outline an efficient strategy for screening heat tolerance and accentuate the need to focus on reduced rates of respiration to improve heat tolerance in rice.
Key messageWe uncouple host and nonhost resistance in barley toPuccinia striiformisff. spp.hordeiandtritici. We isolate, fine map, and physically anchorRps6to chromosome 7H in barley.AbstractA plant may be considered a nonhost of a pathogen if all known genotypes of a plant species are resistant to all known isolates of a pathogen species. However, if a small number of genotypes are susceptible to some known isolates of a pathogen species this plant may be considered an intermediate host. Barley (Hordeum vulgare) is an intermediate host for Puccinia striiformis f. sp. tritici (Pst), the causal agent of wheat stripe rust. We wanted to understand the genetic architecture underlying resistance to Pst and to determine whether any overlap exists with resistance to the host pathogen, Puccinia striiformis f. sp. hordei (Psh). We mapped Pst resistance to chromosome 7H and show that host and intermediate host resistance is genetically uncoupled. Therefore, we designate this resistance locus Rps6. We used phenotypic and genotypic selection on F2:3 families to isolate Rps6 and fine mapped the locus to a 0.1 cM region. Anchoring of the Rps6 locus to the barley physical map placed the region on a single fingerprinted contig spanning a physical region of 267 kb. Efforts are now underway to sequence the minimal tiling path and to delimit the physical region harboring Rps6. This will facilitate additional marker development and permit identification of candidate genes in the region.Electronic supplementary materialThe online version of this article (doi:10.1007/s00122-015-2659-x) contains supplementary material, which is available to authorized users.
Sorghum is a model C4 crop made experimentally tractable by extensive genomic and genetic resources. Biomass sorghum is also studied as a feedstock for biofuel and forage. Mechanistic modelling suggests that reducing stomatal conductance (gs) could improve sorghum intrinsic water use efficiency (iWUE) and biomass production. Phenotyping for discovery of genotype to phenotype associations remain bottlenecks in efforts to understand the mechanistic basis for natural variation in gs and iWUE. This study addressed multiple methodological limitations. Optical tomography and a novel machine learning tool were combined to measure stomatal density (SD). This was combined with rapid measurements of leaf photosynthetic gas exchange and specific leaf area (SLA). These traits were then the subject of genome-wide association study (GWAS) and transcriptome-wide association study (TWAS) across 869 field-grown biomass sorghum accessions. SD was correlated with plant height and biomass production. Plasticity in SD and SLA were interrelated with each other, and productivity, across wet versus dry growing seasons. Moderate-to-high heritability of traits studied across the large mapping population supported identification of associations between DNA sequence variation, or RNA transcript abundance, and trait variation. 394 unique genes underpinning variation in WUE-related traits are described with higher confidence because they were identified in multiple independent tests. This list was enriched in genes whose orthologs in Arabidopsis have functions related to stomatal or leaf development and leaf gas exchange. These advances in methodology and knowledge will aid efforts to improve the WUE of C4 crops.
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