Advances and opportunities in unraveling cold‐tolerance mechanisms in the world’s primary staple food crops

Abstract

Temperatures below or above optimal growth conditions are among the major stressors affecting productivity, end-use quality, and distribution of key staple crops including rice (Oryza sativa), wheat (Triticum aestivum), and maize (Zea mays L.). Among temperature stresses, cold stress induces cellular changes that cause oxidative stress and slowdown metabolism, limit growth, and ultimately reduce crop productivity. Perception of cold stress by plant cells leads to the activation of cold-responsive transcription factors and downstream genes, which ultimately impart cold tolerance. The response triggered in crops to cold stress includes gene expression/suppression, the accumulation of sugars upon chilling, and signaling molecules, among others. Much of the information on the effects of cold stress on perception, signal transduction, gene expression, and plant metabolism are available in the model plant Arabidopsis but somewhat lacking in major crops. Hence, a complete understanding of the molecular mechanisms by which staple crops respond to cold stress remain largely unknown. Here, we make an effort to elaborate on the molecular mechanisms employed in response to low-temperature stress. We summarize the effects of cold stress on the growth and development of these crops, the mechanism of cold perception, and the role of various sensors and transducers in cold signaling. We discuss the progress in cold tolerance research at the genome, transcriptome, proteome, and metabolome levels and highlight how these findings provide opportunities for designing cold-tolerant crops for the future.

Genome‐wide dissection and haplotype analysis identified candidate loci for nitrogen use efficiency under drought conditions in winter wheat

Abstract

Climate change causes extreme conditions like prolonged drought, which results in yield reductions due to its effects on nutrient balances such as nitrogen uptake and utilization by plants. Nitrogen (N) is a crucial nutrient element for plant growth and productivity. Understanding the mechanistic basis of nitrogen use efficiency (NUE) under drought conditions is essential to improve wheat (Triticum aestivum L.) yield. Here, we evaluated the genetic variation of NUE-related traits and photosynthesis response in a diversity panel of 200 wheat genotypes under drought and nitrogen stress conditions to uncover the inherent genetic variation and identify quantitative trait loci (QTLs) underlying these traits. The results revealed significant genetic variations among the genotypes in response to drought stress and nitrogen deprivation. Drought impacted plant performance more than N deprivation due to its effect on water and nutrient uptake. GWAS identified a total of 27 QTLs with a significant main effect on the drought-related traits, while 10 QTLs were strongly associated with the NUE traits. Haplotype analysis revealed two different haplotype blocks within the associated region on chromosomes 1B and 5A. The two haplotypes showed contrasting effects on N uptake and use efficiency traits. The in silico and transcript analyses implicated candidate gene coding for cold shock protein. This gene was the most highly expressed gene under several stress conditions, including drought stress. Upon validation, these QTLs on 1B and 5A could be used as a diagnostic marker for NUE and drought tolerance screening in wheat.

Integrative multi‐omics analyses of date palm (Phoenix dactylifera) roots and leaves reveal how the halophyte land plant copes with sea water

Abstract

Date palm (Phoenix dactylifera L.) is able to grow and complete its life cycle while being rooted in highly saline soils. Which of the many well-known salt-tolerance strategies are combined to fine-tune this remarkable resilience is unknown. The precise location, whether in the shoot or the root, where these strategies are employed remains uncertain, leaving us unaware of how the various known salt-tolerance mechanisms are integrated to fine-tune this remarkable resilience. To address this shortcoming, we exposed date palm to a salt stress dose equivalent to seawater for up to 4 weeks and applied integrative multi-omics analyses followed by targeted metabolomics, hormone, and ion analyses. Integration of proteomic into transcriptomic data allowed a view beyond simple correlation, revealing a remarkably high degree of convergence between gene expression and protein abundance. This sheds a clear light on the acclimatization mechanisms employed, which depend on reprogramming of protein biosynthesis. For growth in highly saline habitats, date palm effectively combines various salt-tolerance mechanisms found in both halophytes and glycophytes: “avoidance” by efficient sodium and chloride exclusion at the roots, and “acclimation” by osmotic adjustment, reactive oxygen species scavenging in leaves, and remodeling of the ribosome-associated proteome in salt-exposed root cells. Combined efficiently as in P. dactylifera L., these sets of mechanisms seem to explain the palm's excellent salt stress tolerance.

Understanding the salt overly sensitive pathway in Prunus: Identification and characterization of NHX, CIPK, and CBL genes

Abstract

Salinity is a major abiotic stress factor that can significantly impact crop growth, and productivity. In response to salt stress, the plant Salt Overly Sensitive (SOS) signaling pathway regulates the homeostasis of intracellular sodium ion concentration. The SOS1, SOS2, and SOS3 genes play critical roles in the SOS pathway, which belongs to the members of Na+/H+ exchanger (NHX), CBL-interacting protein kinase (CIPK), and calcineurin B-like (CBL) gene families, respectively. In this study, we performed genome-wide identifications and phylogenetic analyses of NHX, CIPK, and CBL genes in six Rosaceae species: Prunus persica, Prunus dulcis, Prunus mume, Prunus armeniaca, Pyrus ussuriensis × Pyrus communis, and Rosa chinensis. NHX, CIPK, and CBL genes of Arabidopsis thaliana were used as controls for phylogenetic analyses. Our analysis revealed the lineage-specific and adaptive evolutions of Rosaceae genes. Our observations indicated the existence of two primary classes of CIPK genes: those that are intron-rich and those that are intron-less. Intron-rich CIPKs in Rosaceae and Arabidopsis can be traced back to algae CIPKs and CIPKs found in early plants, suggesting that intron-less CIPKs evolved from their intron-rich counterparts. This study identified one gene for each member of the SOS signaling pathway in P. persica: PpSOS1, PpSOS2, and PpSOS3. Gene expression analyses indicated that all three genes of P. persica were expressed in roots and leaves. Yeast two-hybrid-based protein–protein interaction analyses revealed a direct interaction between PpSOS3 and PpSOS2; and between PpSOS2 and PpSOS1C-terminus region. Our findings indicate that the SOS signaling pathway is highly conserved in P. persica.

What plant breeding may (and may not) look like in 2050?

Abstract

At the turn of 2000 many authors envisioned future plant breeding. Twenty years after, which of those authors’ visions became reality or not, and which ones may become so in the years to come. After two decades of debates, climate change is a “certainty,” food systems shifted from maximizing farm production to reducing environmental impact, and hopes placed into GMOs are mitigated by their low appreciation by consumers. We revise herein how plant breeding may raise or reduce genetic gains based on the breeder's equation. “Accuracy of Selection” has significantly improved by many experimental-scale field and laboratory implements, but also by vulgarizing statistical models, and integrating DNA markers into selection. Pre-breeding has really promoted the increase of useful “Genetic Variance.” Shortening “Recycling Time” has seen great progression, to the point that achieving a denominator equal to “1” is becoming a possibility. Maintaining high “Selection Intensity” remains the biggest challenge, since adding any technology results in a higher cost per progeny, despite the steady reduction in cost per datapoint. Furthermore, the concepts of variety and seed enterprise might change with the advent of cheaper genomic tools to monitor their use and the promotion of participatory or citizen science. The technological and societal changes influence the new generation of plant breeders, moving them further away from field work, emphasizing instead the use of genomic-based selection methods relying on big data. We envisage what skills plant breeders of tomorrow might need to address challenges, and whether their time in the field may dwindle.

Climate change impacts on crop breeding: Targeting interacting biotic and abiotic stresses for wheat improvement

Abstract

Wheat (Triticum aestivum L.) as a staple crop is closely interwoven into the development of modern society. Its influence on culture and economic development is global. Recent instability in wheat markets has demonstrated its importance in guaranteeing food security across national borders. Climate change threatens food security as it interacts with a multitude of factors impacting wheat production. The challenge needs to be addressed with a multidisciplinary perspective delivered across research, private, and government sectors. Many experimental studies have identified the major biotic and abiotic stresses impacting wheat production, but fewer have addressed the combinations of stresses that occur simultaneously or sequentially during the wheat growth cycle. Here, we argue that biotic and abiotic stress interactions, and the genetics and genomics underlying them, have been insufficiently addressed by the crop science community. We propose this as a reason for the limited transfer of practical and feasible climate adaptation knowledge from research projects into routine farming practice. To address this gap, we propose that novel methodology integration can align large volumes of data available from crop breeding programs with increasingly cheaper omics tools to predict wheat performance under different climate change scenarios. Underlying this is our proposal that breeders design and deliver future wheat ideotypes based on new or enhanced understanding of the genetic and physiological processes that are triggered when wheat is subjected to combinations of stresses. By defining this to a trait and/or genetic level, new insights can be made for yield improvement under future climate conditions.

Proteomic analysis of near‐isogenic lines reveals key biomarkers on wheat chromosome 4B conferring drought tolerance

Abstract

Drought is a major constraint for wheat production that is receiving increased attention due to global climate change. This study conducted isobaric tags for relative and absolute quantitation proteomic analysis on near-isogenic lines to shed light on the underlying mechanism of qDSI.4B.1 quantitative trait loci (QTL) on the short arm of chromosome 4B conferring drought tolerance in wheat. Comparing tolerant with susceptible isolines, 41 differentially expressed proteins were identified to be responsible for drought tolerance with a p-value of < 0.05 and fold change >1.3 or <0.7. These proteins were mainly enriched in hydrogen peroxide metabolic activity, reactive oxygen species metabolic activity, photosynthetic activity, intracellular protein transport, cellular macromolecule localization, and response to oxidative stress. Prediction of protein interactions and pathways analysis revealed the interaction between transcription, translation, protein export, photosynthesis, and carbohydrate metabolism as the most important pathways responsible for drought tolerance. The five proteins, including 30S ribosomal protein S15, SRP54 domain-containing protein, auxin-repressed protein, serine hydroxymethyltransferase, and an uncharacterized protein with encoding genes on 4BS, were suggested as candidate proteins responsible for drought tolerance in qDSI.4B.1 QTL. The gene coding SRP54 protein was also one of the differentially expressed genes in our previous transcriptomic study.

Integrated multi‐omics analysis reveals drought stress response mechanism in chickpea (Cicer arietinum L.)

Abstract

Drought is one of the major constraints limiting chickpea productivity. To unravel complex mechanisms regulating drought response in chickpea, we generated transcriptomics, proteomics, and metabolomics datasets from root tissues of four contrasting drought-responsive chickpea genotypes: ICC 4958, JG 11, and JG 11+ (drought-tolerant), and ICC 1882 (drought-sensitive) under control and drought stress conditions. Integration of transcriptomics and proteomics data identified enriched hub proteins encoding isoflavone 4′-O-methyltransferase, UDP-d-glucose/UDP-d-galactose 4-epimerase, and delta-1-pyrroline-5-carboxylate synthetase. These proteins highlighted the involvement of pathways such as antibiotic biosynthesis, galactose metabolism, and isoflavonoid biosynthesis in activating drought stress response mechanisms. Subsequently, the integration of metabolomics data identified six metabolites (fructose, galactose, glucose, myoinositol, galactinol, and raffinose) that showed a significant correlation with galactose metabolism. Integration of root-omics data also revealed some key candidate genes underlying the drought-responsive “QTL-hotspot” region. These results provided key insights into complex molecular mechanisms underlying drought stress response in chickpea.

Whole genome resequencing and phenotyping of MAGIC population for high resolution mapping of drought tolerance in chickpea

Abstract

Terminal drought is one of the major constraints to crop production in chickpea (Cicer arietinum L.). In order to map drought tolerance related traits at high resolution, we sequenced multi-parent advanced generation intercross (MAGIC) population using whole genome resequencing approach and phenotyped it under drought stress environments for two consecutive years (2013–14 and 2014–15). A total of 52.02 billion clean reads containing 4.67 TB clean data were generated on the 1136 MAGIC lines and eight parental lines. Alignment of clean data on to the reference genome enabled identification of a total, 932,172 of SNPs, 35,973 insertions, and 35,726 deletions among the parental lines. A high-density genetic map was constructed using 57,180 SNPs spanning a map distance of 1606.69 cM. Using compressed mixed linear model, genome-wide association study (GWAS) enabled us to identify 737 markers significantly associated with days to 50% flowering, days to maturity, plant height, 100 seed weight, biomass, and harvest index. In addition to the GWAS approach, an identity-by-descent (IBD)-based mixed model approach was used to map quantitative trait loci (QTLs). The IBD-based mixed model approach detected major QTLs that were comparable to those from the GWAS analysis as well as some exclusive QTLs with smaller effects. The candidate genes like FRIGIDA and CaTIFY4b can be used for enhancing drought tolerance in chickpea. The genomic resources, genetic map, marker-trait associations, and QTLs identified in the study are valuable resources for the chickpea community for developing climate resilient chickpeas.

Effect of terminal heat stress on osmolyte accumulation and gene expression during grain filling in bread wheat (Triticum aestivum L.)

Abstract

The grain-filling stage in Triticum aestivum (wheat) is highly vulnerable to increasing temperature as terminal heat stress diminishes grain quality and yield. To examine the mechanism of terminal heat tolerance, we performed the biochemical and gene expression analyses using two heat-tolerant (WH730 and WH1218) and two heat-sensitive (WH711 and WH157) wheat genotypes. We observed a significant increase in total soluble sugar (25%–47%), proline (7%–15%), and glycine betaine (GB) (22%–34%) contents in flag leaf, whereas a decrease in grain-filling duration, 1000-kernel weight (8%–25%), and grain yield per plant (11%–23%) was observed under the late-sown compared to the timely sown. The maximum content of osmolytes, including total soluble sugar, proline, and GB, was observed in heat-tolerant genotypes compared to heat-sensitive genotypes. The expression of 10 heat-responsive genes associated with heat shock proteins (sHsp-1, Hsp17, and HsfA4), flavonoid biosynthesis (F3′-1 and PAL), β-glucan synthesis (CslF6 and CslH), and xyloglucan metabolism (XTH1, XTH2, and XTH5) was studied in flag leaf exposed to different heat treatments (34, 36, 38, and 40°C) at 15 days after anthesis by quantitative real-time polymerase chain reaction. A significant increase in the relative fold expression of these genes with increasing temperature indicated their involvement in providing heat-stress tolerance. The high differential expression of most of the genes in heat-tolerant genotype “WH730” followed by “WH1218” indicates the high adaptability of these genotypes to heat stress compared to heat-sensitive wheat genotypes. Based on the previous results, “WH730” performed better in terms of maximum osmolyte accumulation, grain yield, and gene expression under heat stress.