Willian Batista-Silva

Plant organs harbour diverse components that connect their physiology to the whole organism. The turnover of metabolites may be higher in some organs than in others, triggering differential growth patterns throughout the organism. We revealed that Solanum lycopersicum exhibits more coordinated growth and physiology across the entire plant compared to wild tomato species. Specifically, young leaves of S. lycopersicum develop more slowly than mature leaves, whereas wild species do not exhibit this pattern. Wild tomato Solanum pennellii displays young leaves with higher photosynthetic rates than mature leaves. Consequently, sucrose metabolism in S. pennellii is quite similar between young and mature leaves, while expression patterns of circadian clock genes differ significantly between leaves of different ages. Additionally, we demonstrated that introducing alleles related to tomato domestication into the wild tomato Solanum pimpinellifolium promotes coordinated growth between young and mature leaves, resulting in similar patterns to those observed in S. lycopersicum. Collectively, S. lycopersicum appears to exhibit more coordinated regulation of growth and metabolism, and understanding this process is likely fundamental to explaining its elevated harvest index.

Cells, tissues, and organs harbour complex systems to allow communication between one another. The biological rhythms can be contrasting among organs, tissues, and cells, adjusting the physiology differently along the organism‘s regions. while also synchronising flowering and metabolism. Here, we revealed that Solanum lycopersicum manifests more balanced rhythms across the whole plant than wild tomatoes. Accordingly, the leaf development program is more coordinated in this organism than in wild species, in that young S. lycopersicum leaves develop slowly in comparison to mature leaves. Young leaves from wild tomatoes display higher photosynthetic rate than mature leaves, while large metabolite accumulations occur across plant segments. Consequently, diel metabolite levels are rather similar between young and mature leaves in the wild tomato S. pennellii , whereas the expression patterns for circadian clock genes are widely contrasting between differently aged leaves. We further demonstrated that introduction of domestication alleles into the wild tomato S. pimpinellifolium appears to synchronize the development of young and mature leaves, rendering this similar to that observed for S. lycopersicum . Collectively, the strengthening of inter-organ relationships in S. lycopersicum indicates an increased synchronization of its biology, which is probably fundamental to explain its elevated yield.

SUMMARY: Cells, tissues, and organs are characterized by harbouring complex systems allowing communication between one another. Plant domestication was demonstrated to have structured the circadian rhythms, while also synchronising flowering and metabolism. Here, we demonstrate that the domesticated tomato ( Solanum lycopersicum ) manifests more synchronized rhythmicity across the whole plant. Consequently, the leaf development program is more coordinated in this species than in its wild relatives, wherein S. lycopersicum young leaves develop slowly in comparison to mature leaves. Young leaves from wild tomatoes display higher photosynthesis than mature leaves, while large metabolite accumulations occur across plant segments. Consequently, the diel metabolite levels are rather similar between young and mature leaves in the wild tomato S. pennellii , whereas the expression patterns for circadian clock genes are widely contrasting between both leaves. We further demonstrated that additions of genes related to domestication into the wild tomato S. pimpinellifolium appear to synchronize the development of young and mature leaves to be rather similar to that observed for S. lycopersicum . Collectively, the strengthening of inter-organs relationships on domesticated tomato indicates a synchronized biology, which is most likely fundamental to explaining its elevated yield.

Auxin is an important hormone playing crucial roles during fruit growth and ripening; however, the metabolic impact of changes in auxin signalling during tomato (Solanum lycopersicum L.) ripening remains unclear. Here, we investigated the significance of changes in auxin signalling during different stages of fruit development by analysing changes in tomato fruit quality and primary metabolism using mutants with either lower or higher auxin sensitivity [diageotropica (dgt) and entire mutants, respectively]. Altered auxin sensitivity modifies metabolism, through direct impacts on fruit respiration and fruit growth. We verified that the dgt mutant plants exhibit reductions in fruit set, total fruit dry weight, fruit size, number of seeds per fruit, and fresh weight loss during post-harvest. Sugar accumulation was associated with delayed fruit ripening in dgt, probably connected with reduced ethylene levels and respiration, coupled with a lower rate of starch degradation. In contrast, despite exhibiting parthenocarpy, increased auxin perception (entire) did not alter fruit ripening, leading to only minor changes in primary metabolism. By performing a comprehensive analysis, our results connect auxin signalling and metabolic changes during tomato fruit development, indicating that reduced auxin signalling led to extensive changes in sugar concentration and starch metabolism during tomato fruit ripening.

Auxins are known to regulate xylem development in plants, but their effects on water transport efficiency are poorly known. Here we used tomato plants with the diageotropica mutation (dgt), which has impaired function of a cyclophilin 1 cis–trans isomerase involved in auxin signaling, and the corresponding wild type (WT) to explore the mutation’s effects on plant hydraulics and leaf gas exchange. The xylem of the dgt mutant showed a reduced hydraulically weighted vessel diameter (D_h) (24–43%) and conduit number (25–58%) in petioles and stems, resulting in lower theoretical hydraulic conductivities (K_t); on the other hand, no changes in root D_h and K_t were observed. The measured stem and leaf hydraulic conductances of the dgt mutant were lower (up to 81%), in agreement with the K_t values; however, despite dgt and WT plants showing similar root D_h and K_t, the measured root hydraulic conductance of the dgt mutant was 75% lower. The dgt mutation increased the vein and stomatal density, which could potentially increase photosynthesis. Nevertheless, even though it had the same photosynthetic capacity as WT plants, the dgt mutant showed a photosynthetic rate c. 25% lower, coupled with a stomatal conductance reduction of 52%. These results clearly demonstrate that increases in minor vein and stomatal density only result in higher leaf gas exchange when accompanied by higher hydraulic efficiency.

Hexokinases (HXKs) and fructokinases (FRKs) are the only two families of enzymes in plants that have been identified as able to phosphorylate Glucose (Glc) and Fructose (Fru). Glc can only be phosphorylated in plants by HXKs, while Fru can be phosphorylated by either HXKs or FRKs. The various subcellular localizations of HXKs in plants indicate that they are involved in diverse functions, including anther dehiscence and pollen germination, stomatal closure in response to sugar levels, stomatal aperture and reducing transpiration. Its association with modulating programmed cell death, and responses to oxidative stress and pathogen infection (abiotic and biotic stresses) also have been reported. To extend our understanding about the function of HXK-like genes in the response of Prunus rootstocks to abiotic stress, we performed a detailed bioinformatic and functional analysis of hexokinase 3-like genes (HXK3s) from two Prunus rootstock genotypes, ‘M.2624’ (Prunus cerasifera Ehrh × P. munsoniana W.Wight & Hedrick) and ‘M.F12/1’ (P. avium L.), which are tolerant and sensitive to hypoxia stress, respectively. A previous large-scale transcriptome sequencing of roots of these rootstocks, showed that this HXK3-like gene that was highly induced in the tolerant genotype under hypoxia conditions. In silico analysis of gene promoters from M.2624 and M.F12/1 genotypes revealed regulatory elements that could explain differential transcriptional profiles of HXK3 genes. Subcellular localization was determinates by both bioinformatic prediction and expression of their protein fused to the green fluorescent protein (GFP) in protoplasts and transgenic plants of Arabidopsis. Both approaches showed that they are expressed in plastids. Metabolomics analysis of Arabidopsis plants ectopically expressing Prunus HXK3 genes revealed that content of several metabolites including phosphorylated sugars (G6P), starch and some metabolites associated with the TCA cycle were affected. These transgenic Arabidopsis plants showed improved tolerance to salt and drought stress under growth chamber conditions. Our results suggest that Prunus HXK3 is a potential candidate for enhancing tolerance to salt and drought stresses in stone fruit trees and other plants.

Aluminium is a limiting factor for crop productivity in acidic soils (pH ≤ 5.5). Since acid soil distribution on Earth cannot adequately explain the differential Al tolerance across the plant kingdom, we investigated photoperiod effects on plant Al tolerance. We observed that with increasing distance from the equator, Al tolerance disappears, suggesting a relationship with the photoperiod. Long-day (LD) species are generally more Al-sensitive than short-day (SD) species, whereas genetic conversion of tomato for SD growth boosts Al tolerance. Reduced Al tolerance correlates with DNA-checkpoint activation under LD. DNA-checkpoint-related genes are under positive selection in Arabidopsis accessions from regions with shorter days, suggesting photoperiod acts as a selective barrier for Al tolerance. Our findings revealed that diel regulation and genetic diversity affect Al tolerance, suggesting that day-length orchestrates Al tolerance. One-Sentence Summary: Aluminum is a major constraint for crop yield worldwide. We reveal that photoperiod acts as a barrier for Al tolerance in plants.

Auxin modulates a range of plant developmental processes including embryogenesis, organogenesis, and shoot and root development. Recent studies have shown that plant hormones also strongly influence metabolic networks, which results in altered growth phenotypes. Modulating auxin signalling pathways may therefore provide an opportunity to alter crop performance. Here, we performed a detailed physiological and metabolic characterization of tomato (Solanum lycopersicum) mutants with either increased (entire) or reduced (diageotropica—dgt) auxin signalling to investigate the consequences of altered auxin signalling on photosynthesis, water use, and primary metabolism. We show that reduced auxin sensitivity in dgt led to anatomical and physiological modifications, including altered stomatal distribution along the leaf blade and reduced stomatal conductance, resulting in clear reductions in both photosynthesis and water loss in detached leaves. By contrast, plants with higher auxin sensitivity (entire) increased the photosynthetic capacity, as deduced by higher V_cmax and J_max coupled with reduced stomatal limitation. Remarkably, our results demonstrate that auxin‐sensitive mutants (dgt) are characterized by impairments in the usage of starch that led to lower growth, most likely associated with decreased respiration. Collectively, our findings suggest that mutations in different components of the auxin signalling pathway specifically modulate photosynthetic and respiratory processes.

Malate is a central metabolite involved in a multiplicity of plant metabolic pathways, being associated with mitochondrial metabolism and playing significant roles in stomatal movements. Vacuolar malate transport has been characterized at the molecular level and is performed by at least one carrier protein and two channels in Arabidopsis (Arabidopsis thaliana) vacuoles. The absence of the Arabidopsis tonoplast Dicarboxylate Transporter (tDT) in the tdt knockout mutant was associated previously with an impaired accumulation of malate and fumarate in leaves. Here, we investigated the consequences of this lower accumulation on stomatal behavior and photosynthetic capacity as well as its putative metabolic impacts. Neither the stomatal conductance nor the kinetic responses to dark, light, or high CO₂ were highly affected in tdt plants. In addition, we did not observe any impact on stomatal aperture following incubation with abscisic acid, malate, or citrate. Furthermore, an effect on photosynthetic capacity was not observed in the mutant lines. However, leaf mitochondrial metabolism was affected in the tdt plants. Levels of the intermediates of the tricarboxylic acid cycle were altered, and increases in both light and dark respiration were observed. We conclude that manipulation of the tonoplastic organic acid transporter impacted mitochondrial metabolism, while the overall stomatal and photosynthetic capacity were unaffected.