Daniel Maag

Climate change forces species to adapt rapidly to avoid extinction. To directly observe rapid adaptation and extinction, we conducted synchronized evolution experiments with Arabidopsis thaliana in 30 locations across Western Europe, the Mediterranean, the Levant, and North America. Whole-genome pooled sequencing of ~70,000 surviving plants revealed repeatable allele frequency shifts in similar climates but divergent shifts across contrasting ones, indicating evolutionary adaptation. We identified genetic variants linked to climate adaptation, including genes involved in processes ranging from thermal-stress sensing to spring-flowering timing. Evolutionary trends were often predictable, but variable, across environments. In warmer climates, evolutionary predictability correlated with population survival over 5 years, whereas erratic changes preceded extinction. These results show that rapid climate adaptation is possible, but understanding its limits will be crucial for biodiversity forecasting.

Plants exhibit considerable phenotypic plasticity, allowing them to adapt their metabolism to the fluctuating energy supply in a natural environment. Using dark-induced senescence (DIS) as an experimental system, a mutant study combining phenotypic, transcriptomic and chromatin immunoprecipitation sequencing approaches identified distinct members of the Arabidopsis thaliana group S1 basic leucine zipper (bZIP) transcription factors that orchestrate the starvation response. Whereas excluding bZIP2, bZIP11, and bZIP44 to play a major role in DIS, bZIP1, and bZIP53 act partially redundantly to control a coexpression network governing amino acid catabolism and transport, gluconeogenesis and energy homeostasis. Moreover, bZIP1 and bZIP53 regulate genes involved in the asparagine–glutamine balance, two amino acids critical for carbon and nitrogen homeostasis. This transcriptional reprogramming in resource management is required for survival during starvation and regaining meristematic activity during the recovery from stress. Thus, our findings provide insights into the transcriptional control of plant resource and energy management during starvation. Overall, this work sheds light on the discrepancy between in vitro DNA binding and overexpression studies versus mutant analyses and in vivo DNA binding, providing a critical view on how to define specific transcription factor functions within large families.

Plants respond to elevated temperatures with enhanced elongation growth that depends on rapid transcriptional, post-transcriptional, and post-translational reprogramming. However, it is unclear how temperature information integrates with the splicing machinery to establish warm temperature-dependent splicing patterns. In animals, CDC2-LIKE KINASES (CLKs) function as body temperature sensors that control temperature-dependent splicing via phosphorylation of serine/arginine-rich (SR) proteins. Here we demonstrate that the CLK-homologous ARABIDOPSIS FUS3-COMPLEMENTING (AFC) kinases likewise regulate post-transcriptional RNA processing to control warm temperature-dependent growth in Arabidopsis. The contrasting temperature-activity profiles of the three AFCs depend on specific structural elements, including a conserved activation segment within the kinase domain. Combining protein structure prediction with site-directed mutagenesis, we provide insights into structural features that determine the different temperature-activity profiles of the three AFC paralogs. Analyses of afc mutant plants demonstrate their role in establishing temperature-dependent splicing patterns and thermomorphogenic hypocotyl elongation. Finally, our data indicate SR34 and SR34a as phosphorylation targets mediating temperature-dependent hypocotyl elongation downstream of AFCs. In conclusion, our study provides evidence that temperature-controlled AFC activity is evolutionarily conserved between plants and animals and implicates AFCs in the control of thermomorphogenesis.

Plants exhibit an immense plasticity in their architecture. While the impact of hormonal regulation is well-characterised, the importance of sugar-signalling has just recently emerged. Here, we addressed which sugar-signalling components mediate the trade-off between growth of apical versus lateral meristems and how they control organ sink-strength. Thereby, we unravelled a novel developmental function of the sugar-controlled S ₁ basic-leucine-zipper (S ₁ -bZIP) transcription factors in establishing global source-sink interactions. Applying comprehensive molecular, analytical, and genetic approaches, we demonstrate that S ₁ -bZIPs operate in a redundant manner to control tissue-specific expression of defined SWEET sugar-transporters and the GAT1_2.1 glutaminase. By these means, S ₁ -bZIPs control carbohydrate (C)-channelling from source leaves to apical shoot and root organs and tune systemic organic nitrogen (N)-supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.

High temperature stress limits plant growth and reproduction. Exposure to high temperature, however, also elicits a conserved physiological response, which protects plants from the damage evoked by heat. This response involves a partial reconfiguration of the plant metabolome including the accumulation of the trisaccharide raffinose. In this study, we explored the intra-specific variation of warm temperature-induced raffinose accumulation as a metabolic marker for temperature responsiveness with the aim to identify genes that contribute to plant thermotolerance. By combining raffinose measurements in 250 Arabidopsis thaliana accessions following a mild heat treatment with genome-wide association studies we identified five genomic regions that were associated with the observed trait variation. Subsequent functional analyses confirmed a causal relationship between TREHALOSE-6-PHOSPHATE SYNTHASE 1 ( TPS1 ) and warm temperature-dependent raffinose synthesis. Moreover, complementation of the tps1-1 null mutant with functionally distinct TPS1 isoforms differentially affected carbohydrate metabolism under more severe heat stress. While higher TPS1 activity was associated with reduced endogenous sucrose levels and thermotolerance, disruption of trehalose 6-phosphate signalling resulted in higher accumulation of transitory starch and sucrose and was associated with enhanced heat resistance. Taken together, our findings suggest a role of trehalose 6-phosphate in thermotolerance most likely through its regulatory function in carbon partitioning and sucrose homeostasis.

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti‐predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re‐attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish‐fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate‐deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti‐predator defense needs to be further evaluated in the field.

Summary: The induced production of secondary metabolites in herbivore‐attacked plants varies in space and time. However, the consequences of these spatiotemporal patterns for herbivore performance are not well understood. This is particularly true for 1,4‐benzoxazin‐3‐ones (BXs), the major induced defensive metabolites of maize. Here we report on the spatiotemporal dynamics of BX induction and its consequences for the leaf feeder Spodoptera littoralis. Defence‐related phytohormones and transcript levels of BX biosynthetic genes were upregulated locally at the wound site within 12 h of herbivory. Within another 12 h, the insecticidal BX HDMBOA‐Glc started to accumulate in a highly localized manner at the feeding site. Changes in BX metabolism away from the feeding site within the same leaf were much weaker and were undetected in systemic leaves. Following the removal of the caterpillars, local HDMBOA‐Glc levels remained elevated for 7 days. Caterpillars that were forced to feed directly on locally induced leaf parts, but not on adjacent leaf parts, suffered from reduced growth. This effect was abolished in the BX‐deficient bx1 mutant. We did not find any evidence that BXs regulate defensive phytohormones or their own accumulation. In summary, this study shows that induced herbivore resistance in maize is highly localized and dependent on BXs.

A genome-wide quantitative trait mapping strategy revealed a side branch of the benzoxazinoid pathway in maize that specifically increases maize resistance agai

As a consequence of artificial selection for specific traits, crop plants underwent considerable genotypic and phenotypic changes during the process of domestication. These changes may have led to reduced resistance in the cultivated plant due to shifts in resource allocation from defensive traits to increased growth rates and yield. Modern maize (Zea mays ssp. mays) was domesticated from its ancestor Balsas teosinte (Z. mays ssp. parviglumis) approximately 9000 years ago. Although maize displays a high genetic overlap with its direct ancestor and other annual teosintes, several studies show that maize and its ancestors differ in their resistance phenotypes with teosintes being less susceptible to herbivore damage. However, the underlying mechanisms are poorly understood. Here we addressed the question to what extent maize domestication has affected two crucial chemical and one physical defence traits and whether differences in their expression may explain the differences in herbivore resistance levels. The ontogenetic trajectories of 1,4-benzoxazin-3-ones, maysin and leaf toughness were monitored for different leaf types across several maize cultivars and teosinte accessions during early vegetative growth stages. We found significant quantitative and qualitative differences in 1,4-benzoxazin-3-one accumulation in an initial pairwise comparison, but we did not find consistent differences between wild and cultivated genotypes during a more thorough examination employing several cultivars/accessions. Yet, 1,4-benzoxazin-3-one levels tended to decline more rapidly with plant age in the modern maize cultivars. Foliar maysin levels and leaf toughness increased with plant age in a leaf-specific manner, but were also unaffected by domestication. Based on our findings we suggest that defence traits other than the ones that were investigated are responsible for the observed differences in herbivore resistance between teosinte and maize. Furthermore, our results indicate that single pairwise comparisons may lead to false conclusions regarding the effects of domestication on defensive and possibly other traits.