ABSTRACT
In Northern Europe, sowing maize one-month earlier than current agricultural practices may lead to moderate chilling damage. However, studies of the metabolic responses to low, non-freezing, temperatures remain scarce. Here, genetically-diverse maize hybrids (Zea mays, dent inbred lines crossed with a flint inbred line) were cultivated in a growth chamber at optimal temperature and then three decreasing temperatures for 2 days each, as well as in the field. Leaf metabolomic and proteomic profiles were determined. In the growth chamber, 50% of metabolites and 18% of proteins changed between 20 and 16°C. These maize responses, partly differing from those of Arabidopsis to short-term chilling, were mapped on genome-wide metabolic maps. Several metabolites and proteins showed similar variation for all temperature decreases: seven MS-based metabolite signatures and two proteins involved in photosynthesis decreased continuously. Several increasing metabolites or proteins in the growth-chamber chilling conditions showed similar trends in the early-sowing field experiment, including trans-aconitate, three hydroxycinnamate derivatives, a benzoxazinoid, a sucrose synthase, lethal leaf-spot 1 protein, an allene oxide synthase, several glutathione transferases and peroxidases. Hybrid groups based on field biomass were used to search for the metabolite or protein responses differentiating them in growth-chamber conditions, which could be of interest for breeding.
Subject(s)
Arabidopsis/metabolism , Cold-Shock Response/physiology , Metabolome , Proteome/metabolism , Zea mays/metabolism , Zea mays/physiology , Cold Temperature , Genotype , Phenotype , Photosynthesis , Plant Leaves/physiology , Plant Proteins/metabolism , Zea mays/geneticsABSTRACT
Maize can grow in cool temperate climates but is often exposed to spring chilling temperatures that can affect early seedling growth. Here, we used two sister double-haploid lines displaying a contrasted tolerance to chilling to identify major determinants of long-term chilling tolerance. The chilling-sensitive (CS) and the chilling-tolerant (CT) lines were grown at 14 °C day/10 °C night for 60 d. CS plants displayed a strong reduction in growth and aerial biomass compared with CT plants. Photosynthetic efficiency was affected with an increase in energy dissipation in both lines. Chilling tolerance in CT plants was associated with higher chlorophyll content, glucose-6-phosphate dehydrogenase activity, and higher sucrose to starch ratio. Few changes in cell wall composition were observed in both genotypes. There was no obvious correlation between nucleotide sugar content and cell wall polysaccharide composition. Our findings suggest that the central starch-sucrose metabolism is one major determinant of the response to low temperature, and its modulation accounts for the ability of CT plants to cope with low temperature. This modulation seemed to be linked to a strong alteration in the biosynthesis of nucleotide sugars that, at a high level, could reflect the remobilization of carbon in response to chilling.
Subject(s)
Carbon/metabolism , Cold Temperature , Zea mays/metabolism , Adaptation, Physiological/genetics , Zea mays/geneticsABSTRACT
INTRODUCTION: In Northern Europe, maize early-sowing used to maximize yield may lead to moderate damages of seedlings due to chilling without visual phenotypes. Genetic studies and breeding for chilling tolerance remain necessary, and metabolic markers would be particularly useful in this context. OBJECTIVES: Using an untargeted metabolomic approach on a collection of maize hybrids, our aim was to identify metabolite signatures and/or metabolites associated with chilling responses at the vegetative stage, to search for metabolites differentiating groups of hybrids based on silage-earliness, and to search for marker-metabolites correlated with aerial biomass. METHODS: Thirty genetically-diverse maize dent inbred-lines (Zea mays) crossed to a flint inbred-line were sown in a field to assess metabolite profiles upon cold treatment induced by a modification of sowing date, and characterized with climatic measurements and phenotyping. RESULTS: NMR- and LC-MS-based metabolomic profiling revealed the biological variation of primary and specialized metabolites in young leaves of plants before flowering-stage. The effect of early-sowing on leaf composition was larger than that of genotype, and several metabolites were associated to sowing response. The metabolic distances between genotypes based on leaf compositional data were not related to the genotype admixture groups, and their variability was lower under early-sowing than normal-sowing. Several metabolites or metabolite-features were related to silage-earliness groups in the normal-sowing condition, some of which were confirmed the following year. Correlation networks involving metabolites and aerial biomass suggested marker-metabolites for breeding for chilling tolerance. CONCLUSION: After validation in other experiments and larger genotype panels, these marker-metabolites can contribute to breeding.
Subject(s)
Metabolomics , Plant Breeding , Zea mays/metabolism , Biomarkers/metabolism , Chromatography, Liquid , Phenotype , Proton Magnetic Resonance Spectroscopy , Spectrometry, Mass, Electrospray IonizationABSTRACT
BACKGROUND: European Flint maize inbred lines are used as a source of adaptation to cold in most breeding programs in Northern Europe. A deep understanding of their adaptation strategy could thus provide valuable clues for further improvement, which is required in the current context of climate change. We therefore compared six inbreds and two derived Flint x Dent hybrids for their response to one-week at low temperature (10 °C day/7 or 4 °C night) during steady-state vegetative growth. RESULTS: Leaf growth was arrested during chilling treatment but recovered fast upon return to warm temperature, so that no negative effect on shoot biomass was measured. Gene expression analyses of the emerging leaf in the hybrids suggest that plants maintained a 'ready-to-grow' state during chilling since cell cycle genes were not differentially expressed in the division zone and genes coding for expansins were on the opposite up-regulated in the elongation zone. In photosynthetic tissues, a strong reduction in PSII efficiency was measured. Chilling repressed chlorophyll biosynthesis; we detected accumulation of the precursor geranylgeranyl chlorophyll a and down-regulation of GERANYLGERANYL REDUCTASE (GGR) in mature leaf tissues. Excess light energy was mostly dissipated through fluorescence and constitutive thermal dissipation processes, rather than by light-regulated thermal dissipation. Consistently, only weak clues of xanthophyll cycle activation were found. CO2 assimilation was reduced by chilling, as well as the expression levels of genes encoding phosphoenolpyruvate carboxylase (PEPC), pyruvate orthophosphate dikinase (PPDK), and the small subunit of Rubisco. Accumulation of sugars was correlated with a strong decrease of the specific leaf area (SLA). CONCLUSIONS: Altogether, our study reveals good tolerance of the photosynthetic machinery of Northern European maize to chilling and suggests that growth arrest might be their strategy for fast recovery after a mild stress.
Subject(s)
Cold Temperature , Stress, Physiological/physiology , Zea mays/physiology , Adaptation, Physiological , Plant Breeding , Plant Leaves/genetics , Plant Leaves/physiology , Zea mays/geneticsABSTRACT
BACKGROUND: Breeding for cold tolerance in maize promises to allow increasing growth area and production in temperate zones. The objective of this research was to conduct genome-wide association analyses (GWAS) in temperate maize inbred lines and to find strategies for pyramiding genes for cold tolerance. Two panels of 306 dent and 292 European flint maize inbred lines were evaluated per se and in testcrosses under cold and control conditions in a growth chamber. We recorded indirect measures for cold tolerance as the traits number of days from sowing to emergence, relative leaf chlorophyll content or quantum efficiency of photosystem II. Association mapping for identifying genes associated to cold tolerance in both panels was based on genotyping with 49,585 genome-wide single nucleotide polymorphism (SNP) markers. RESULTS: We found 275 significant associations, most of them in the inbreds evaluated per se, in the flint panel, and under control conditions. A few candidate genes coincided between the current research and previous reports. A total of 47 flint inbreds harbored the favorable alleles for six significant quantitative trait loci (QTL) detected for inbreds per se evaluated under cold conditions, four of them had also the favorable alleles for the main QTL detected from the testcrosses. Only four dent inbreds (EZ47, F924, NK807 and PHJ40) harbored the favorable alleles for three main QTL detected from the evaluation of the dent inbreds per se under cold conditions. There were more QTL in the flint panel and most of the QTL were associated with days to emergence and ΦPSII. CONCLUSIONS: These results open new possibilities to genetically improve cold tolerance either with genome-wide selection or with marker assisted selection.
Subject(s)
Cold Temperature , Stress, Physiological/genetics , Zea mays/genetics , Alleles , Chromosome Mapping , Chromosomes, Plant/genetics , Crosses, Genetic , Genome-Wide Association Study , Genotype , Linkage Disequilibrium/genetics , Polymorphism, Single Nucleotide/genetics , Quantitative Trait Loci/geneticsABSTRACT
Maize (Zea mays L.) is one of the major cereal crops in the world and is highly sensitive to low temperature. Here, changes in photosynthetic and cell wall metabolisms were investigated during a long chilling exposure in inbred line F2 and a low-lignin near-isogenic brown midrib3 mutant (F2bm3), which has a mutation in the caffeic acid O-methyltransferase (COMT) gene. Results revealed that the plant biomass was reduced, and this was more pronounced in F2bm3. Photosynthesis was altered in both lines with distinct changes in photosynthetic pigment content between F2bm3 and F2, indicating an alternative photoprotection mechanism between lines under chilling. Starch remobilization was observed in F2bm3 while concentrations of sucrose, fructose and starch increased in F2, suggesting a reduced sugar partitioning in F2. The cell wall was altered upon chilling, resulting in changes in the composition of glucuronorabinoxylan and a reduced cellulose level in F2. Chilling shifted lignin subunit composition in F2bm3 mutant to a higher proportion of p-hydroxyphenyl (H) units, whereas it resulted in lignin with a higher proportion of syringyl (S) residues in F2. On average, the total cell wall ferulic acid (FA) content increased in both genotypes, with an increase in ether-linked FA in F2bm3, suggesting a greater degree of cross-linking to lignin. The reinforcement of the cell wall with lignin enriched in H-units and a higher concentration in cell-wall-bound FA observed in F2bm3 as a response to chilling, could be a strategy to protect the photosystems.
Subject(s)
Lignin , Zea mays , Cell Wall/metabolism , Lignin/metabolism , Photosynthesis/genetics , Starch/metabolism , Zea mays/genetics , Zea mays/metabolismABSTRACT
*In this study, we examined the impact of transient chilling in maize (Zea mays). We investigated the respective roles of the direct effects of stressing temperatures and indirect whorl size-mediated effects on the growth of leaves chilled at various stages of development. *Cell production, individual leaf extension and final leaf size of plants grown in a glasshouse under three temperature regimes (a control and two short chilling transfers) were studied using two genotypes contrasting in terms of their architecture. *The kinetics of all the leaves emerging after the stress were affected, but not all final leaf lengths were affected. No size-mediated propagation of an initial growth reduction was observed, but a size-mediated effect was associated with a longer duration of leaf elongation which compensated for reduced leaf elongation rates when leaves were stressed during their early growth. Both cell division and cell expansion contributed to explaining cold-induced responses at the leaf level. *These results demonstrate that leaf elongation kinetics and final leaf length are under the control of processes at the n - 1 (cell proliferation and expansion) and n + 1 (whorl size signal) scales. Both levels may respond to chilling stress with different time lags, making it possible to buffer short-term responses.
Subject(s)
Cold Temperature , Plant Leaves/anatomy & histology , Plant Leaves/growth & development , Stress, Physiological , Zea mays/anatomy & histology , Zea mays/growth & development , Cell Count , Cell Size , Kinetics , Models, Biological , Organ Size , Plant Epidermis/cytology , Plant Leaves/cytology , Time Factors , Zea mays/cytologyABSTRACT
BACKGROUND: In the last decade, metabolomics has emerged as a powerful diagnostic and predictive tool in many branches of science. Researchers in microbes, animal, food, medical and plant science have generated a large number of targeted or non-targeted metabolic profiles by using a vast array of analytical methods (GC-MS, LC-MS, 1H-NMR .). Comprehensive analysis of such profiles using adapted statistical methods and modeling has opened up the possibility of using single or combinations of metabolites as markers. Metabolic markers have been proposed as proxy, diagnostic or predictors of key traits in a range of model species and accurate predictions of disease outbreak frequency, developmental stages, food sensory evaluation and crop yield have been obtained. AIM OF REVIEW: (i) To provide a definition of plant performance and metabolic markers, (ii) to highlight recent key applications involving metabolic markers as tools for monitoring or predicting plant performance, and (iii) to propose a workable and cost-efficient pipeline to generate and use metabolic markers with a special focus on plant breeding. KEY MESSAGE: Using examples in other models and domains, the review proposes that metabolic markers are tending to complement and possibly replace traditional molecular markers in plant science as efficient estimators of performance.
ABSTRACT
Flowering time is a major adaptive trait in plants and an important selection criterion for crop species. In maize, however, little is known about its molecular basis. In this study, we report the fine mapping and characterization of a major quantitative trait locus located on maize chromosome 10, which regulates flowering time through photoperiod sensitivity. This study was performed in near-isogenic material derived from a cross between the day-neutral European flint inbred line FV286 and the tropical short-day inbred line FV331. Recombinant individuals were identified among a large segregating population and their progenies were scored for flowering time. Combined genotypic characterization led to delimit the QTL to an interval of 170 kb and highlighted an unbalanced recombination pattern. Two bacterial artificial chromosomes (BACs) covering the region were analyzed to identify putative candidate genes, and synteny with rice, sorghum, and brachypodium was investigated. A gene encoding a CCT domain protein homologous to the rice Ghd7 heading date regulator was identified, but its causative role was not demonstrated and deserves further analyses. Finally, an association study showed a strong level of linkage disequilibrium over the region and highlighted haplotypes that could provide useful information for the exploitation of genetic resources and marker-assisted selection in maize.
Subject(s)
Chromosome Mapping , Chromosomes, Plant/genetics , Flowers/genetics , Haplotypes , Quantitative Trait Loci , Zea mays/genetics , Genes, Plant/genetics , Genetic Variation , Genome-Wide Association Study , Molecular Sequence Data , Reproducibility of Results , Synteny , Time FactorsABSTRACT
Maize (Zea mays L.) is a chill-susceptible crop cultivated in northern latitude environments. The detrimental effects of cold on growth and photosynthetic activity have long been established. However, a general overview of how important these processes are with respect to the reduction of productivity reported in the field is still lacking. In this study, a model-assisted approach was used to dissect variations in productivity under suboptimal temperatures and quantify the relative contributions of light interception (PARc) and radiation use efficiency (RUE) from emergence to flowering. A combination of architectural and light transfer models was used to calculate light interception in three field experiments with two cold-tolerant lines and at two sowing dates. Model assessment confirmed that the approach was suitable to infer light interception. Biomass production was strongly affected by early sowings. RUE was identified as the main cause of biomass reduction during cold events. Furthermore, PARc explained most of the variability observed at flowering, its relative contributions being more or less important according to the climate experienced. Cold temperatures resulted in lower PARc, mainly because final leaf length and width were significantly reduced for all leaves emerging after the first cold occurrence. These results confirm that virtual plants can be useful as fine phenotyping tools. A scheme of action of cold on leaf expansion, light interception and radiation use efficiency is discussed with a view towards helping breeders define relevant selection criteria.