Meeting the global food demand of the future by engineering crop photosynthesis and yield potential.

Increase in demand for our primary foodstuffs is outstripping increase in yields, an expanding gap that indicates large potential food shortages by mid-century. This comes at a time when yield improvements are slowing or stagnating as the approaches of the Green Revolution reach their biological limits. Photosynthesis, which has been improved little in crops and falls far short of its biological limit, emerges as the key remaining route to increase the genetic yield potential of our major crops. Thus, there is a timely need to accelerate our understanding of the photosynthetic process in crops to allow informed and guided improvements via in-silico-assisted genetic engineering. Potential and emerging approaches to improving crop photosynthetic efficiency are discussed, and the new tools needed to realize these changes are presented.

Optimal nitrogen rate strategy for sustainable rice production in China.

Avoiding excessive agricultural nitrogen (N) use without compromising yields has long been a priority for both research and government policy in China1,2. Although numerous rice-related strategies have been proposed3-5, few studies have assessed their impacts on national food self-sufficiency and environmental sustainability and fewer still have considered economic risks faced by millions of smallholders. Here we established an optimal N rate strategy based on maximizing either economic (ON) or ecological (EON) performance using new subregion-specific models. Using an extensive on-farm dataset, we then assessed the risk of yield losses among smallholder farmers and the challenges of implementing the optimal N rate strategy. We find that meeting national rice production targets in 2030 is possible while concurrently reducing nationwide N consumption by 10% (6-16%) and 27% (22-32%), mitigating reactive N (Nr) losses by 7% (3-13%) and 24% (19-28%) and increasing N-use efficiency by 30% (3-57%) and 36% (8-64%) for ON and EON, respectively. This study identifies and targets subregions with disproportionate environmental impacts and proposes N rate strategies to limit national Nr pollution below proposed environmental thresholds, without compromising soil N stocks or economic benefits for smallholders. Thereafter, the preferable N strategy is allocated to each region based on the trade-off between economic risk and environmental benefit. To facilitate the adoption of the annually revised subregional N rate strategy, several recommendations were provided, including a monitoring network, fertilization quotas and smallholder subsidies.

The giant diploid faba genome unlocks variation in a global protein crop.

Increasing the proportion of locally produced plant protein in currently meat-rich diets could substantially reduce greenhouse gas emissions and loss of biodiversity1. However, plant protein production is hampered by the lack of a cool-season legume equivalent to soybean in agronomic value2. Faba bean (Vicia faba L.) has a high yield potential and is well suited for cultivation in temperate regions, but genomic resources are scarce. Here, we report a high-quality chromosome-scale assembly of the faba bean genome and show that it has expanded to a massive 13 Gb in size through an imbalance between the rates of amplification and elimination of retrotransposons and satellite repeats. Genes and recombination events are evenly dispersed across chromosomes and the gene space is remarkably compact considering the genome size, although with substantial copy number variation driven by tandem duplication. Demonstrating practical application of the genome sequence, we develop a targeted genotyping assay and use high-resolution genome-wide association analysis to dissect the genetic basis of seed size and hilum colour. The resources presented constitute a genomics-based breeding platform for faba bean, enabling breeders and geneticists to accelerate the improvement of sustainable protein production across the Mediterranean, subtropical and northern temperate agroecological zones.

Reducing brassinosteroid signalling enhances grain yield in semi-dwarf wheat.

Modern green revolution varieties of wheat (Triticum aestivum L.) confer semi-dwarf and lodging-resistant plant architecture owing to the Reduced height-B1b (Rht-B1b) and Rht-D1b alleles1. However, both Rht-B1b and Rht-D1b are gain-of-function mutant alleles encoding gibberellin signalling repressors that stably repress plant growth and negatively affect nitrogen-use efficiency and grain filling2-5. Therefore, the green revolution varieties of wheat harbouring Rht-B1b or Rht-D1b usually produce smaller grain and require higher nitrogen fertilizer inputs to maintain their grain yields. Here we describe a strategy to design semi-dwarf wheat varieties without the need for Rht-B1b or Rht-D1b alleles. We discovered that absence of Rht-B1 and ZnF-B (encoding a RING-type E3 ligase) through a natural deletion of a haploblock of about 500 kilobases shaped semi-dwarf plants with more compact plant architecture and substantially improved grain yield (up to 15.2%) in field trials. Further genetic analysis confirmed that the deletion of ZnF-B induced the semi-dwarf trait in the absence of the Rht-B1b and Rht-D1b alleles through attenuating brassinosteroid (BR) perception. ZnF acts as a BR signalling activator to facilitate proteasomal destruction of the BR signalling repressor BRI1 kinase inhibitor 1 (TaBKI1), and loss of ZnF stabilizes TaBKI1 to block BR signalling transduction. Our findings not only identified a pivotal BR signalling modulator but also provided a creative strategy to design high-yield semi-dwarf wheat varieties by manipulating the BR signal pathway to sustain wheat production.

Abiotic stress responses in plants.

Plants cannot move, so they must endure abiotic stresses such as drought, salinity and extreme temperatures. These stressors greatly limit the distribution of plants, alter their growth and development, and reduce crop productivity. Recent progress in our understanding of the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications. This improved knowledge can be used to boost crop productivity and agricultural sustainability through genetic, chemical and microbial approaches.

Global trends of cropland phosphorus use and sustainability challenges.

To meet the growing food demand while addressing the multiple challenges of exacerbating phosphorus (P) pollution and depleting P rock reserves1-15, P use efficiency (PUE, the ratio of productive P output to P input in a defined system) in crop production needs to be improved. Although many efforts have been devoted to improving nutrient management practices on farms, few studies have examined the historical trajectories of PUE and their socioeconomic and agronomic drivers on a national scale1,2,6,7,11,16,17. Here we present a database of the P budget (the input and output of the crop production system) and PUE by country and by crop type for 1961-2019, and examine the substantial contribution of several drivers for PUE, such as economic development stages and crop portfolios. To address the P management challenges, we found that global PUE in crop production must increase to 68-81%, and recent trends indicate some meaningful progress towards this goal. However, P management challenges and opportunities in croplands vary widely among countries.

Genomic basis of geographical adaptation to soil nitrogen in rice.

The intensive application of inorganic nitrogen underlies marked increases in crop production, but imposes detrimental effects on ecosystems1,2: it is therefore crucial for future sustainable agriculture to improve the nitrogen-use efficiency of crop plants. Here we report the genetic basis of nitrogen-use efficiency associated with adaptation to local soils in rice (Oryza sativa L.). Using a panel of diverse rice germplasm collected from different ecogeographical regions, we performed a genome-wide association study on the tillering response to nitrogen-the trait that is most closely correlated with nitrogen-use efficiency in rice-and identified OsTCP19 as a modulator of this tillering response through its transcriptional response to nitrogen and its targeting to the tiller-promoting gene DWARF AND LOW-TILLERING (DLT)3,4. A 29-bp insertion and/or deletion in the OsTCP19 promoter confers a differential transcriptional response and variation in the tillering response to nitrogen among rice varieties. The allele of OsTCP19 associated with a high tillering response to nitrogen is prevalent in wild rice populations, but has largely been lost in modern cultivars: this loss correlates with increased local soil nitrogen content, which suggests that it might have contributed to geographical adaptation in rice. Introgression of the allele associated with a high tillering response into modern rice cultivars boosts grain yield and nitrogen-use efficiency under low or moderate levels of nitrogen, which demonstrates substantial potential for rice breeding and the amelioration of negative environment effects by reducing the application of nitrogen to crops.

Understanding the Genetic Basis of C4 Kranz Anatomy with a View to Engineering C3 Crops.

One of the most remarkable examples of convergent evolution is the transition from C3 to C4 photosynthesis, an event that occurred on over 60 independent occasions. The evolution of C4 is particularly noteworthy because of the complexity of the developmental and metabolic changes that took place. In most cases, compartmentalized metabolic reactions were facilitated by the development of a distinct leaf anatomy known as Kranz. C4 Kranz anatomy differs from ancestral C3 anatomy with respect to vein spacing patterns across the leaf, cell-type specification around veins, and cell-specific organelle function. Here we review our current understanding of how Kranz anatomy evolved and how it develops, with a focus on studies that are dissecting the underlying genetic mechanisms. This research field has gained prominence in recent years because understanding the genetic regulation of Kranz may enable the C3-to-C4 transition to be engineered, an endeavor that would significantly enhance crop productivity.

A comprehensive quantification of global nitrous oxide sources and sinks.

Nitrous oxide (N2O), like carbon dioxide, is a long-lived greenhouse gas that accumulates in the atmosphere. Over the past 150 years, increasing atmospheric N2O concentrations have contributed to stratospheric ozone depletion1 and climate change2, with the current rate of increase estimated at 2 per cent per decade. Existing national inventories do not provide a full picture of N2O emissions, owing to their omission of natural sources and limitations in methodology for attributing anthropogenic sources. Here we present a global N2O inventory that incorporates both natural and anthropogenic sources and accounts for the interaction between nitrogen additions and the biochemical processes that control N2O emissions. We use bottom-up (inventory, statistical extrapolation of flux measurements, process-based land and ocean modelling) and top-down (atmospheric inversion) approaches to provide a comprehensive quantification of global N2O sources and sinks resulting from 21 natural and human sectors between 1980 and 2016. Global N2O emissions were 17.0 (minimum-maximum estimates: 12.2-23.5) teragrams of nitrogen per year (bottom-up) and 16.9 (15.9-17.7) teragrams of nitrogen per year (top-down) between 2007 and 2016. Global human-induced emissions, which are dominated by nitrogen additions to croplands, increased by 30% over the past four decades to 7.3 (4.2-11.4) teragrams of nitrogen per year. This increase was mainly responsible for the growth in the atmospheric burden. Our findings point to growing N2O emissions in emerging economies-particularly Brazil, China and India. Analysis of process-based model estimates reveals an emerging N2O-climate feedback resulting from interactions between nitrogen additions and climate change. The recent growth in N2O emissions exceeds some of the highest projected emission scenarios3,4, underscoring the urgency to mitigate N2O emissions.

Climate-resilient crops: Lessons from xerophytes.

Developing climate-resilient crops is critical for future food security and sustainable agriculture under current climate scenarios. Of specific importance are drought and soil salinity. Tolerance traits to these stresses are highly complex, and the progress in improving crop tolerance is too slow to cope with the growing demand in food production unless a major paradigm shift in crop breeding occurs. In this work, we combined bioinformatics and physiological approaches to compare some of the key traits that may differentiate between xerophytes (naturally drought-tolerant plants) and mesophytes (to which the majority of the crops belong). We show that both xerophytes and salt-tolerant mesophytes have a much larger number of copies in key gene families conferring some of the key traits related to plant osmotic adjustment, abscisic acid (ABA) sensing and signalling, and stomata development. We show that drought and salt-tolerant species have (i) higher reliance on Na for osmotic adjustment via more diversified and efficient operation of Na+ /H+ tonoplast exchangers (NHXs) and vacuolar H+ - pyrophosphatase (VPPases); (ii) fewer and faster stomata; (iii) intrinsically lower ABA content; (iv) altered structure of pyrabactin resistance/pyrabactin resistance-like (PYR/PYL) ABA receptors; and (v) higher number of gene copies for protein phosphatase 2C (PP2C) and sucrose non-fermenting 1 (SNF1)-related protein kinase 2/open stomata 1 (SnRK2/OST1) ABA signalling components. We also show that the past trends in crop breeding for Na+ exclusion to improve salinity stress tolerance are counterproductive and compromise their drought tolerance. Incorporating these genetic insights into breeding practices could pave the way for more drought-tolerant and salt-resistant crops, securing agricultural yields in an era of climate unpredictability.

Metabolite-mediated adaptation of crops to drought and the acquisition of tolerance.

Drought is one of the major and growing threats to agriculture productivity and food security. Metabolites are involved in the regulation of plant responses to various environmental stresses, including drought stress. The complex drought tolerance can be ascribed to several simple metabolic traits. These traits could then be used for detecting the genetic architecture of drought tolerance. Plant metabolomes show dynamic differences when drought occurs during different developmental stages or upon different levels of drought stress. Here, we reviewed the major and most recent findings regarding the metabolite-mediated plant drought response. Recent progress in the development of drought-tolerant agents is also discussed. We provide an updated schematic overview of metabolome-driven solutions for increasing crop drought tolerance and thereby addressing an impending agricultural challenge.

Kinetic modeling identifies targets for engineering improved photosynthetic efficiency in potato (Solanum tuberosum cv. Solara).

Potato (Solanum tuberosum) is a significant non-grain food crop in terms of global production. However, its yield potential might be raised by identifying means to release bottlenecks within photosynthetic metabolism, from the capture of solar energy to the synthesis of carbohydrates. Recently, engineered increases in photosynthetic rates in other crops have been directly related to increased yield - how might such increases be achieved in potato? To answer this question, we derived the photosynthetic parameters Vcmax and Jmax to calibrate a kinetic model of leaf metabolism (e-Photosynthesis) for potato. This model was then used to simulate the impact of manipulating the expression of genes and their protein products on carbon assimilation rates in silico through optimizing resource investment among 23 photosynthetic enzymes, predicting increases in photosynthetic CO2 uptake of up to 67%. However, this number of manipulations would not be practical with current technologies. Given a limited practical number of manipulations, the optimization indicated that an increase in amounts of three enzymes - Rubisco, FBP aldolase, and SBPase - would increase net assimilation. Increasing these alone to the levels predicted necessary for optimization increased photosynthetic rate by 28% in potato.

A carboxysome-based CO2 concentrating mechanism for C3 crop chloroplasts: advances and the road ahead.

The introduction of the carboxysome-based CO2 concentrating mechanism (CCM) into crop plants has been modelled to significantly increase crop yields. This projection serves as motivation for pursuing this strategy to contribute to global food security. The successful implementation of this engineering challenge is reliant upon the transfer of a microcompartment that encapsulates cyanobacterial Rubisco, known as the carboxysome, alongside active bicarbonate transporters. To date, significant progress has been achieved with respect to understanding various aspects of the cyanobacterial CCM, and more recently, different components of the carboxysome have been successfully introduced into plant chloroplasts. In this Perspective piece, we summarise recent findings and offer new research avenues that will accelerate research in this field to ultimately and successfully introduce the carboxysome into crop plants for increased crop yields.

Thirty years of resistance: Zig-zag through the plant immune system.

Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 . Since then, many cell-surface pattern recognition receptors (PRRs) have been identified, and R genes that encode intracellular nucleotide-binding leucine-rich repeat receptors (NLRs) have been cloned. Here, we provide a list of characterized PRRs and NLRs. In addition to immune receptors, many components of immune signaling networks were discovered over the last 30 years. We review the signaling pathways, physiological responses, and molecular regulation of both PRR- and NLR-mediated immunity. Recent studies have reinforced the importance of interactions between the two immune systems. We provide an overview of interactions between PRR- and NLR-mediated immunity, highlighting challenges and perspectives for future research.

Comparative transcriptomic analysis provides insights into the genetic networks regulating oil differential production in oil crops.

BACKGROUND: Plants differ more than threefold in seed oil contents (SOCs). Soybean (Glycine max), cotton (Gossypium hirsutum), rapeseed (Brassica napus), and sesame (Sesamum indicum) are four important oil crops with markedly different SOCs and fatty acid compositions. RESULTS: Compared to grain crops like maize and rice, expanded acyl-lipid metabolism genes and relatively higher expression levels of genes involved in seed oil synthesis (SOS) in the oil crops contributed to the oil accumulation in seeds. Here, we conducted comparative transcriptomics on oil crops with two different SOC materials. In common, DIHYDROLIPOAMIDE DEHYDROGENASE, STEAROYL-ACYL CARRIER PROTEIN DESATURASE, PHOSPHOLIPID:DIACYLGLYCEROL ACYLTRANSFERASE, and oil-body protein genes were both differentially expressed between the high- and low-oil materials of each crop. By comparing functional components of SOS networks, we found that the strong correlations between genes in "glycolysis/gluconeogenesis" and "fatty acid synthesis" were conserved in both grain and oil crops, with PYRUVATE KINASE being the common factor affecting starch and lipid accumulation. Network alignment also found a conserved clique among oil crops affecting seed oil accumulation, which has been validated in Arabidopsis. Differently, secondary and protein metabolism affected oil synthesis to different degrees in different crops, and high SOC was due to less competition of the same precursors. The comparison of Arabidopsis mutants and wild type showed that CINNAMYL ALCOHOL DEHYDROGENASE 9, the conserved regulator we identified, was a factor resulting in different relative contents of lignins to oil in seeds. The interconnection of lipids and proteins was common but in different ways among crops, which partly led to differential oil production. CONCLUSIONS: This study goes beyond the observations made in studies of individual species to provide new insights into which genes and networks may be fundamental to seed oil accumulation from a multispecies perspective.

Leaf anatomy does not explain the large variability of mesophyll conductance across C3 crop species.

Increasing mesophyll conductance of CO2 (gm ) is a strategy to improve photosynthesis in C3 crops. However, the relative importance of different anatomical traits in determining gm in crops is unclear. Mesophyll conductance measurements were performed on 10 crops using the online carbon isotope discrimination method and the 'variable J' method in parallel. The influences of crucial leaf anatomical traits on gm were evaluated using a one-dimensional anatomical CO2 diffusion model. The gm values measured using two independent methods were compatible, although significant differences were observed in their absolute values. Quantitative analysis showed that cell wall thickness and chloroplast stroma thickness are the most important elements along the diffusion pathway. Unexpectedly, the large variability of gm across crops was not associated with any investigated leaf anatomical traits except chloroplast thickness. The gm values estimated using the anatomical model differed remarkably from the values measured in vivo in most species. However, when the species-specific effective porosity of the cell wall and the species-specific facilitation effect of CO2 diffusion across the membrane and chloroplast stoma were taken into account, the model could output gm values very similar to those measured in vivo. These results indicate that gm variation across crops is probably also driven by the effective porosity of the cell wall and effects of facilitation of CO2 transport across the membrane and chloroplast stroma in addition to the thicknesses of the elements.

The transcriptome of soybean reproductive tissues subjected to water deficit, heat stress, and a combination of water deficit and heat stress.

Global warming and climate change are driving an alarming increase in the frequency and intensity of extreme climate events, such as droughts, heat waves, and their combination, inflicting heavy losses to agricultural production. Recent studies revealed that the transcriptomic responses of different crops to water deficit (WD) or heat stress (HS) are very different from that to a combination of WD + HS. In addition, it was found that the effects of WD, HS, and WD + HS are significantly more devastating when these stresses occur during the reproductive growth phase of crops, compared to vegetative growth. As the molecular responses of different reproductive and vegetative tissues of plants to WD, HS, or WD + HS could be different from each other and these differences could impact many current and future attempts to enhance the resilience of crops to climate change through breeding and/or engineering, we conducted a transcriptomic analysis of different soybean (Glycine max) tissues to WD, HS, and WD + HS. Here we present a reference transcriptomic dataset that includes the response of soybean leaf, pod, anther, stigma, ovary, and sepal to WD, HS, and WD + HS conditions. Mining this dataset for the expression pattern of different stress response transcripts revealed that each tissue had a unique transcriptomic response to each of the different stress conditions. This finding is important as it suggests that enhancing the overall resilience of crops to climate change could require a coordinated approach that simultaneously alters the expression of different groups of transcripts in different tissues in a stress-specific manner.

Exploring selection signatures in the divergence and evolution of lipid droplet (LD) associated genes in major oilseed crops.

BACKGROUND: Oil bodies or lipid droplets (LDs) in the cytosol are the subcellular storage compartments of seeds and the sites of lipid metabolism providing energy to the germinating seeds. Major LD-associated proteins are lipoxygenases, phospholipaseD, oleosins, TAG-lipases, steroleosins, caleosins and SEIPINs; involved in facilitating germination and enhancing peroxidation resulting in off-flavours. However, how natural selection is balancing contradictory processes in lipid-rich seeds remains evasive. The present study was aimed at the prediction of selection signatures among orthologous clades in major oilseeds and the correlation of selection effect with gene expression. RESULTS: The LD-associated genes from the major oil-bearing crops were analyzed to predict natural selection signatures in phylogenetically close-knit ortholog clusters to understand adaptive evolution. Positive selection was the major force driving the evolution and diversification of orthologs in a lineage-specific manner. Significant positive selection effects were found in 94 genes particularly in oleosin and TAG-lipases, purifying with excess of non-synonymous substitution in 44 genes while 35 genes were neutral to selection effects. No significant selection impact was noticed in Brassicaceae as against LOX genes of oil palm. A heavy load of deleterious mutations affecting selection signatures was detected in T-lineage oleosins and LOX genes of Arachis hypogaea. The T-lineage oleosin genes were involved in mainly anther, tapetum and anther wall morphogenesis. In Ricinus communis and Sesamum indicum > 85% of PLD genes were under selection whereas selection pressures were low in Brassica juncea and Helianthus annuus. Steroleosin, caleosin and SEIPINs with large roles in lipid droplet organization expressed mostly in seeds and were under considerable positive selection pressures. Expression divergence was evident among paralogs and homeologs with one gene attaining functional superiority compared to the other. The LOX gene Glyma.13g347500 associated with off-flavor was not expressed during germination, rather its paralog Glyma.13g347600 showed expression in Glycine max. PLD-α genes were expressed on all the tissues except the seed,δ genes in seed and meristem while ß and γ genes expressed in the leaf. CONCLUSIONS: The genes involved in seed germination and lipid metabolism were under strong positive selection, although species differences were discernable. The present study identifies suitable candidate genes enhancing seed oil content and germination wherein directional selection can become more fruitful.

Revisiting Changes in Growth, Physiology and Stress Responses of Plants under the Effect of Enhanced CO2 and Temperature.

Climate change has universally affected the whole ecosystem in a unified manner and is known to have improbable effects on agricultural productivity and food security. Carbon dioxide (CO2) and temperature are the major environmental factors that have been shown to increase sharply during the last century and are directly responsible for affecting plant growth and development. A number of previous investigations have deliberated the positive effects of elevated CO2 on plant growth and development of various C3 crops, while detrimental effects of enhanced temperature on different crop plants like rice, wheat, maize and legumes are generally observed. A combined effect of elevated CO2 and temperature has yet to be studied in great detail; therefore, this review attempts to delineate the interactive effects of enhanced CO2 and temperature on plant growth, development, physiological and molecular responses. Elevated CO2 maintains leaf photosynthesis rate, respiration, transpiration and stomatal conductance in the presence of elevated temperature and sustains plant growth and productivity in the presence of both these environmental factors. Concomitantly, their interaction also affects the nutritional quality of seeds and leads to alterations in the composition of secondary metabolites. Elevated CO2 and temperature modulate phytohormone concentration in plants, and due to this fact, both environmental factors have substantial effects on abiotic and biotic stresses. Elevated CO2 and temperature have been shown to have mitigating effects on plants in the presence of other abiotic stress agents like drought and salinity, while no such pattern has been observed in the presence of biotic stress agents. This review focuses on the interactive effects of enhanced CO2 and temperature on different plants and is the first of its kind to deliver their combined responses in such detail.