Water availability influences all aspects of plant growth and development; however, most studies of plant responses to drought have focused on vegetative organs, notably roots and leaves. Far less is known about the molecular bases of drought acclimation responses in fruits, which are complex organs with distinct tissue types. To obtain a more comprehensive picture of the molecular mechanisms governing fruit development under drought, we profiled the transcriptomes of a spectrum of fruit tissues from tomato (Solanum lycopersicum), spanning early growth through ripening and collected from plants grown under varying intensities of water stress. In addition, we compared transcriptional changes in fruit with those in leaves to highlight different and conserved transcriptome signatures in vegetative and reproductive organs. We observed extensive and diverse genetic reprogramming in different fruit tissues and leaves, each associated with a unique response to drought acclimation. These included major transcriptional shifts in the placenta of growing fruit and in the seeds of ripe fruit related to cell growth and epigenetic regulation, respectively. Changes in metabolic and hormonal pathways, such as those related to starch, carotenoids, jasmonic acid, and ethylene metabolism, were associated with distinct fruit tissues and developmental stages. Gene coexpression network analysis provided further insights into the tissue-specific regulation of distinct responses to water stress. Our data highlight the spatiotemporal specificity of drought responses in tomato fruit and indicate known and unrevealed molecular regulatory mechanisms involved in drought acclimation, during both vegetative and reproductive stages of development.
Tomato (Solanum lycopersicum) fruit store carbon as starch during early development and mobilize it at the onset of ripening. Starch accumulation has been suggested to buffer fluctuations in carbon supply to the fruit under abiotic stress, and contribute to sugar levels in ripe fruit. However, the role of starch accumulation and metabolism during fruit development is still unclear. Here we show that the tomato mutant adpressa (adp) harbors a mutation in a gene encoding the small subunit of ADP-glucose pyrophosphorylase that abolishes starch synthesis. The disruption of starch biosynthesis causes major transcriptional and metabolic remodeling in adp fruit but only minor effects on fruit size and ripening. Changes in gene expression and metabolite profiles indicate that the lack of carbon flow into starch increases levels of soluble sugars during fruit growth, triggers a readjustment of central carbohydrate and lipid metabolism, and activates growth and stress protection pathways. Accordingly, adp fruits are remarkably resistant to blossom-end rot, a common physiological disorder induced by environmental stress. Our results provide insights into the effects of perturbations of carbohydrate metabolism on tomato fruit development, with potential implications for the enhancement of protective mechanisms against abiotic stress in fleshy fruit.
more » « less- NSF-PAR ID:
- 10472826
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 74
- Issue:
- 20
- ISSN:
- 0022-0957
- Format(s):
- Medium: X Size: p. 6331-6348
- Size(s):
- ["p. 6331-6348"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
SUMMARY As sessile organisms, plants encounter dynamic and challenging environments daily, including abiotic/biotic stresses. The regulation of carbon and nitrogen allocations for the synthesis of plant proteins, carbohydrates, and lipids is fundamental for plant growth and adaption to its surroundings. Light, one of the essential environmental signals, exerts a substantial impact on plant metabolism and resource partitioning (i.e., starch). However, it is not fully understood how light signaling affects carbohydrate production and allocation in plant growth and development. An orphan gene unique to
Arabidopsis thaliana , namedQUA‐QUINE STARCH (QQS ) is involved in the metabolic processes for partitioning of carbon and nitrogen among proteins and carbohydrates, thus influencing leaf, seed composition, and plant defense in Arabidopsis. In this study, we show that PHYTOCHROME‐INTERACTING bHLH TRANSCRIPTION FACTORS (PIFs), including PIF4, are required to suppressQQS during the period at dawn, thus preventing overconsumption of starch reserves.QQS expression is significantly de‐repressed inpif4 andpifQ , while repressed by overexpression ofPIF4 , suggesting that PIF4 and its close homologs (PIF1, PIF3, and PIF5) act as negative regulators ofQQS expression. In addition, we show that the evening complex, including ELF3 is required for active expression ofQQS , thus playing a positive role in starch catabolism during night‐time. Furthermore,QQS is epigenetically suppressed by DNA methylation machinery, whereas histone H3 K4 methyltransferases (e.g., ATX1, ATX2, and ATXR7) and H3 acetyltransferases (e.g., HAC1 and HAC5) are involved in the expression ofQQS . This study demonstrates that PIF light signaling factors help plants utilize optimal amounts of starch during the night and prevent overconsumption of starch before its biosynthesis during the upcoming day. -
more » « less
Abstract Enhancing crop yields is a major challenge because of an increasing human population, climate change, and reduction in arable land. Here, we demonstrate that long-lasting growth enhancement and increased stress tolerance occur by pretreatment of dark grown Arabidopsis seedlings with ethylene before transitioning into light. Plants treated this way had longer primary roots, more and longer lateral roots, and larger aerial tissue and were more tolerant to high temperature, salt, and recovery from hypoxia stress. We attributed the increase in plant growth and stress tolerance to ethylene-induced photosynthetic-derived sugars because ethylene pretreatment caused a 23% increase in carbon assimilation and increased the levels of glucose (266%), sucrose/trehalose (446%), and starch (87%). Metabolomic and transcriptomic analyses several days posttreatment showed a significant increase in metabolic processes and gene transcripts implicated in cell division, photosynthesis, and carbohydrate metabolism. Because of this large effect on metabolism, we term this “ethylene-mediated metabolic priming.” Reducing photosynthesis with inhibitors or mutants prevented the growth enhancement, but this was partially rescued by exogenous sucrose, implicating sugars in this growth phenomenon. Additionally, ethylene pretreatment increased the levels of CINV1 and CINV2 encoding invertases that hydrolyze sucrose, and cinv1;cinv2 mutants did not respond to ethylene pretreatment with increased growth indicating increased sucrose breakdown is critical for this trait. A model is proposed where ethylene-mediated metabolic priming causes long-term increases in photosynthesis and carbohydrate utilization to increase growth. These responses may be part of the natural development of seedlings as they navigate through the soil to emerge into light.
-
Plant organs and tissues are comprised of an array of cell types often superimposed on a gradient of developmental stages. As a result, the ability to analyze and understand the synthesis, metabolism, and accumulation of plant biomolecules requires improved methods for cell- and tissue-specific analysis. Tomato (Solanum lycopersicum) is the world’s most valuable fruit crop and is an important source of health-promoting dietary compounds, including carotenoids. Furthermore, tomato possesses unique genetic activities at the cell and tissue levels, making it an ideal system for tissue- and cell-type analysis of important biochemicals. A sample preparation workflow was developed for cell-type-specific carotenoid analysis in tomato fruit samples. Protocols for hyperspectral imaging of tomato fruit samples, cryoembedding and sectioning of pericarp tissue, laser microdissection of specific cell types, metabolite extraction using cell wall digestion enzymes and pressure cycling, and carotenoid quantification by supercritical fluid chromatography were optimized and integrated into a working protocol. The workflow was applied to quantify carotenoids in the cuticle and noncuticle component of the tomato pericarp during fruit development from the initial ripening to full ripe stages. Carotenoids were extracted and quantified from cell volumes less than 10 nL. This workflow for cell-type-specific metabolite extraction and quantification can be adapted for the analysis of diverse metabolites, cell types, and organismsmore » « less
-
Semrau, Jeremy D. (Ed.)ABSTRACT Food crops are grown with fertilizers containing nitrogen, phosphorus, and potassium (macronutrients) along with magnesium, calcium, boron, and zinc (micronutrients) at different ratios during their cultivation. Soil and plant-associated microbes have been implicated to promote plant growth, stress tolerance, and productivity. However, the high degree of variability across agricultural environments makes it difficult to assess the possible influences of nutrient fertilizers on these microbial communities. Uncovering the underlying mechanisms could lead us to achieve consistently improved food quality and productivity with minimal environmental impacts. For this purpose, we tested a commercially available fertilizer (surface-mined volcanic ash deposit Azomite) applied as a supplement to the normal fertilizer program of greenhouse-grown tomato plants. Because this treatment showed a significant increase in fruit production at measured intervals, we examined its impact on the composition of below-ground microbial communities, focusing on members identified as “core taxa” that were enriched in the rhizosphere and root endosphere compared to bulk soil and appeared above their predicted neutral distribution levels in control and treated samples. This analysis revealed that Azomite had little effect on microbial composition overall, but it had a significant, temporally selective influence on the core taxa. Changes in the composition of the core taxa were correlated with computationally inferred changes in functional pathway enrichment associated with carbohydrate metabolism, suggesting a shift in available microbial nutrients within the roots. This finding exemplifies how the nutrient environment can specifically alter the functional capacity of root-associated bacterial taxa, with the potential to improve crop productivity. IMPORTANCE Various types of soil fertilizers are used routinely to increase crop yields globally. The effects of these treatments are assessed mainly by the benefits they provide in increased crop productivity. There exists a gap in our understanding of how soil fertilizers act on the plant-associated microbial communities. The underlying mechanisms of nutrient uptake are widely complex and, thus, difficult to evaluate fully but have critical influences on both soil and plant health. Here, we presented a systematic approach to analyzing the effects of fertilizer on core microbial communities in soil and plants, leading to predictable outcomes that can be empirically tested and used to develop simple and affordable field tests. The methods described here can be used for any fertilizer and crop system. Continued effort in advancing our understanding of how fertilizers affect plant and microbe relations is needed to advance scientific understanding and help growers make better-informed decisions.more » « less
