C4 photosynthesis outperforms the ancestral C3 state in a wide range of natural and agro-ecosystems by affording higher water-use and nitrogen-use efficiencies. It therefore represents a prime target for engineering novel, high-yielding crops by introducing the trait into C3 backgrounds. However, the genetic architecture of C4 photosynthesis remains largely unknown. To define the divergence in gene expression modules between C3 and C4 photosynthesis during leaf ontogeny, we generated comprehensive transcriptome atlases of two Cleomaceae species, Gynandropsis gynandra (C4) and Tarenaya hassleriana (C3), by RNA sequencing. Overall, the gene expression profiles appear remarkably similar between the C3 and C4 species. We found that known C4 genes were recruited to photosynthesis from different expression domains in C3, including typical housekeeping gene expression patterns in various tissues as well as individual heterotrophic tissues. Furthermore, we identified a structure-related module recruited from the C3 root. Comparison of gene expression patterns with anatomy during leaf ontogeny provided insight into genetic features of Kranz anatomy. Altered expression of developmental factors and cell cycle genes is associated with a higher degree of endoreduplication in enlarged C4 bundle sheath cells. A delay in mesophyll differentiation apparent both in the leaf anatomy and the transcriptome allows for extended vein formation in the C4 leaf.
Summary Root exudation is a key plant function with a large influence on soil organic matter dynamics and plant–soil feedbacks in forest ecosystems. Yet despite its importance, the main ecological drivers of root exudation in mature forest trees remain to be identified. During two growing seasons, we analyzed the dependence of in situ collected root exudates on root morphology, soil chemistry and nutrient availability in six mature European beech (Fagus sylvatica L.) forests on a broad range of bedrock types. Root morphology was a major driver of root exudation across the nutrient availability gradient. A doubling of specific root length exponentially increased exudation rates of mature trees by c. 5‐fold. Root exudation was also closely negatively related to soil pH and nitrogen (N) availability. At acidic and N‐poor sites, where fungal biomass was reduced, exudation rates were c. 3‐fold higher than at N‐ and base‐richer sites and correlated negatively with the activity of enzymes degrading less bioavailable carbon (C) and N in the bulk soil. We conclude that root exudation increases on highly acidic, N‐poor soils, in which fungal activity is reduced and a greater portion of the assimilated plant C is shifted to the external ecosystem C cycle.
Cyanidioschyzon merolae (C. merolae) is an acidophilic red alga growing in a naturally low carbon dioxide (CO) environment. Although it uses a ribulose 1,5-bisphosphate carboxylase/oxygenase with high affinity for CO, the survival of C. merolae relies on functional photorespiratory metabolism. In this study, we quantified the transcriptomic response of C. merolae to changes in CO conditions. We found distinct changes upon shifts between CO conditions, such as a concerted up-regulation of photorespiratory genes and responses to carbon starvation. We used the transcriptome data set to explore a hypothetical CO concentrating mechanism in C. merolae, based on the assumption that photorespiratory genes and possible candidate genes involved in a CO concentrating mechanism are co-expressed. A putative bicarbonate transport protein and two α-carbonic anhydrases were identified, which showed enhanced transcript levels under reduced CO conditions. Genes encoding enzymes of a PEPCK-type C pathway were co-regulated with the photorespiratory gene cluster. We propose a model of a hypothetical low CO compensation mechanism in C. merolae integrating these low CO-inducible components.
Crassulacean acid metabolism (CAM) has evolved as a water-saving strategy, and its engineering into crops offers an opportunity to improve their water use efficiency. This requires a comprehensive understanding of the regulation of the CAM pathway. Here, we use the facultative CAM species Talinum triangulare as a model in which CAM can be induced rapidly by exogenous abscisic acid. RNA sequencing and metabolite measurements were employed to analyse the changes underlying CAM induction and identify potential CAM regulators. Non-negative matrix factorization followed by k-means clustering identified an early CAM-specific cluster and a late one, which was specific for the early light phase. Enrichment analysis revealed abscisic acid metabolism, WRKY-regulated transcription, sugar and nutrient transport, and protein degradation in these clusters. Activation of the CAM pathway was supported by up-regulation of phosphoenolpyruvate carboxylase, cytosolic and chloroplastic malic enzymes, and several transport proteins, as well as by increased end-of-night titratable acidity and malate accumulation. The transcription factors HSFA2, NF-YA9, and JMJ27 were identified as candidate regulators of CAM induction. With this study we promote the model species T. triangulare, in which CAM can be induced in a controlled way, enabling further deciphering of CAM regulation.
C4 species have evolved more than 60 times independently from C3 ancestors. This multiple and parallel evolution of the complex C4 trait indicates common underlying evolutionary mechanisms that might be identified by comparative analysis of closely related C3 and C4 species. Efficient C4 function depends on a distinctive leaf anatomy that is characterized by enlarged, chloroplast rich bundle sheath cells and a narrow vein spacing. To elucidate molecular mechanisms generating this so called Kranz anatomy, we analyzed a developmental series of leaves from the C4 plant Flaveria bidentis and the closely related C3 species Flaveria robusta using leaf clearing and whole transcriptome sequencing. Applying non-negative matrix factorization on the data identified four different zones with distinct transcriptome patterns in growing leaves of both species. Comparing these transcriptome patterns revealed an important role of auxin metabolism and especially auxin homeostasis for establishing the high vein density typical for C4 leaves.2012). Under current ambient CO2 concentrations (405 ppm) at 25°C, photorespiration is estimated to decrease the yield of soybean or wheat in the US by 36% and 20%, respectively (Walker et al., 2016). Environmental constrains such as high temperatures and drought further increases Rubisco oxygenase activity (Laing et al., 1974; Jordan and Ogren, 1984; Brooks and Farquhar, 1985; Parry et al., 2007).In most C4 plants CO2 fixation is compartmentalized between two cell types, the bundle sheath (BS) and the mesophyll (M) cells. In the mesophyll phosphoenolpyruvate (PEP) is carboxylated by phosphoenolpyruvate carboxylase (PEPC), resulting in the 4-carbon compound oxaloacetate (OAA). OAA is converted to malate and/or aspartate, which is then transferred to the bundle sheath. Here the 4-carbon compounds are decarboxylated and the released CO2 is assimilated in the Calvin-Benson-Bassham cycle (CBB). The resulting pyruvate is transferred back to the mesophyll where the primary CO2 acceptor PEP is regenerated by pyruvate orthophosphate dikinase (PPDK) (Hatch, 1987).C4 photosynthesis requires a particular leaf anatomy. As BS and M cells operate as a photosynthetic unit, direct contact of both cell types is necessary to ensure efficient photosynthesis.The BS is composed of the cells directly adjacent to the vasculature. Therefore, leaves of most C4 species exhibit high vein densities with a characteristic pattern in which two veins, each surrounded by BS cells, are separated by only two layers of M cells in a vein-bundle sheathmesophyll-mesophyll-bundle sheath-vein layout. Bundle sheath cells of C4 plants often appear larger in cross-section compared to C3 species and contain more chloroplasts. This character-
Summary Aureochromes represent a unique type of blue light photoreceptors that possess a blue light sensing flavin-binding LOV-domain and a DNA-binding bZIP domain, thus being light-driven transcription factors. The diatom Phaeodactylum tricornutum , a member of the essential marine primary producers, possesses four aureochromes (PtAUREO1a, 1b, 1c, 2). Here we show a dramatic change in the global gene expression pattern of P. tricornutum wild-type cells after a shift from red to blue light. About 75% of the genes show significantly changed transcript levels already after 10 and 60 min of blue light exposure, which includes genes of major transcription factors as well as other photoreceptors. Very surprisingly, this light-induced regulation of gene expression is almost completely inhibited in independent PtAureo1a knockout lines. Such a massive and fast transcriptional change depending on one single photoreceptor is so far unprecedented. We conclude that PtAUREO1a plays a key role in diatoms upon blue light exposure.
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