Desiccation tolerance (DT) is a remarkable process that allows seeds in the dry state to remain viable for long periods of time that in some instances exceed 1,000 y. It has been postulated that seed DT evolved by rewiring the regulatory and signaling networks that controlled vegetative DT, which itself emerged as a crucial adaptive trait of early land plants. Understanding the networks that regulate seed desiccation tolerance in model plant systems would provide the tools to understand an evolutionary process that played a crucial role in the diversification of flowering plants. In this work, we used an integrated approach that included genomics, bioinformatics, metabolomics, and molecular genetics to identify and validate molecular networks that control the acquisition of DT in Arabidopsis seeds. Two DT-specific transcriptional subnetworks were identified related to storage of reserve compounds and cellular protection mechanisms that act downstream of the embryo development master regulators LEAFY COTYLEDON 1 and 2, FUSCA 3, and ABSCICIC ACID INSENSI-TIVE 3. Among the transcription factors identified as major nodes in the DT regulatory subnetworks, PLATZ1, PLATZ2, and AGL67 were confirmed by knockout mutants and overexpression in a desiccationintolerant mutant background to play an important role in seed DT. Additionally, we found that constitutive expression of PLATZ1 in WT plants confers partial DT in vegetative tissues.regulatory network | desiccation tolerance | drought tolerance | seed development | oligosaccharides D esiccation tolerance (DT) can be operationally defined as the ability of an organism to dry to equilibrium with moderately dry air (50 to 70% relative humidity at 20 to 30°C) and then resume normal function when rehydrated (1). DT organisms orchestrate a complex number of responses to protect cellular structures and prevent damage to proteins and nucleic acids. Early land plants evolved mechanisms to survive harsh drying environments to successfully exploit different ecosystems on land. Therefore, it has been postulated that the initial evolution of vegetative DT, in both vegetative and reproductive stages, was a crucial step required for the colonization of land by primitive plants of a fresh water origin (2).Seed DT, a trait that allows terrestrial plants to survive long periods of sparse water until favorable conditions are present for germination, is probably part of the answer to Darwin's "abominable mystery," the sudden appearance of great angiosperm diversity in the fossil record. In angiosperms, DT is acquired at the seed maturation stage, which involves a complex regulatory network (3, 4) that activates a large subset of genes involved in a number of mechanisms that influence seed survival in the dry state. The set of genes required for seed DT includes genes encoding protective proteins such as late embryogenesis abundant (LEA) (5, 6) and heat shock proteins (HSPs) (7), enzymes involved in scavenging reactive oxygen species (8) and the biosynthesis of protective compounds such as o...
Background Desiccation tolerant Selaginella species evolved to survive extreme environmental conditions. Studies to determine the mechanisms involved in the acquisition of desiccation tolerance (DT) have focused on only a few Selaginella species. Due to the large diversity in morphology and the wide range of responses to desiccation within the genus, the understanding of the molecular basis of DT in Selaginella species is still limited. Results Here we present a reference transcriptome for the desiccation tolerant species S. sellowii and the desiccation sensitive species S. denticulata. The analysis also included transcriptome data for the well-studied S. lepidophylla (desiccation tolerant), in order to identify DT mechanisms that are independent of morphological adaptations. We used a comparative approach to discriminate between DT responses and the common water loss response in Selaginella species. Predicted proteomes show strong homology, but most of the desiccation responsive genes differ between species. Despite such differences, functional analysis revealed that tolerant species with different morphologies employ similar mechanisms to survive desiccation. Significant functions involved in DT and shared by both tolerant species included induction of antioxidant systems, amino acid and secondary metabolism, whereas species-specific responses included cell wall modification and carbohydrate metabolism. Conclusions Reference transcriptomes generated in this work represent a valuable resource to study Selaginella biology and plant evolution in relation to DT. Our results provide evidence of convergent evolution of S. sellowii and S. lepidophylla due to the different gene sets that underwent selection to acquire DT
Achieving sustainable agriculture and producing enough food for the increasing global population will require effective strategies to cope with harsh environments such as water and nutrient stress, high temperatures and compacted soils with high impedance that drastically reduce crop yield. Recent advances in the understanding of the molecular, cellular and epigenetic mechanisms that orchestrate plant responses to abiotic stress will serve as the platform to engineer improved crop plants with better designed root system architecture and optimized metabolism to enhance water and nutrients uptake and use efficiency and/or soil penetration. In this review we discuss such advances and how the generated knowledge could be used to integrate effective strategies to engineer crops by gene transfer or genome editing technologies.
Improving phosphorus (P) crop nutrition has emerged as a key factor toward achieving a more resilient and sustainable agriculture. P is an essential nutrient for plant development and reproduction, and phosphate (Pi)-based fertilizers represent one of the pillars that sustain food production systems. To meet the global food demand, the challenge for modern agriculture is to increase food production and improve food quality in a sustainable way by significantly optimizing Pi fertilizer use efficiency. The development of genetically improved crops with higher Pi uptake and Pi-use efficiency and higher adaptability to environments with low-Pi availability will play a crucial role toward this end. In this review, we summarize the current understanding of Pi nutrition and the regulation of Pi-starvation responses in plants, and provide new perspectives on how to harness the ample repertoire of genetic mechanisms behind these adaptive responses for crop improvement. We discuss on the potential of implementing more integrative, versatile, and effective strategies by incorporating systems biology approaches and tools such as genome editing and synthetic biology. These strategies will be invaluable for producing high-yielding crops that require reduced Pi fertilizer inputs and to develop a more sustainable global agriculture.
While most plants die below a threshold of water content, desiccation-tolerant species display specific responses that allow them to survive extreme dehydration. Some of these responses are activated at critical stages during water loss and could represent the difference between desiccation tolerance (DT) and death. Here, we report the development of a simple and reproducible system to determine DT in Selaginella species. The system is based on exposure of excised tissue to a dehydration agent inside small containers, and subsequent evaluation for tissue viability. We evaluated several methodologies to determine viability upon desiccation including: triphenyltetrazolium chloride (TTC) staining, the quantum efficiency of photosystem II, antioxidant potential and relative electrolyte leakage. Our results show that the TTC test is a simple and accurate assay to identify novel desiccation-tolerant Selaginella species, and can also indicate viability in other desiccation-tolerant models (i.e., ferns and mosses). The system we developed is particularly useful to identify critical points during the dehydration process. We found that a desiccation-sensitive Selaginella species show a change in viability when dehydrated to 40% RWC, indicating the onset of a critical condition at this water content. Comparative studies at critical stages could provide a better understanding of DT mechanisms and unravel insights into the key responses to survive desiccation.
In the context of plant evolution, pteridophytes, which is comprised of lycophytes and ferns, occupy an intermediate position between bryophytes and seed plants, sharing characteristics with both groups. Pteridophytes is a highly diverse group of plant species that occupy a wide range of habitats including ecosystems with extreme climatic conditions. There is a significant number of pteridophytes that can tolerate desiccation by temporarily arresting their metabolism in the dry state and reactivating it upon rehydration. Desiccation-tolerant pteridophytes exhibit a strategy that appears to be intermediate between the constitutive and inducible desiccation tolerance (DT) mechanisms observed in bryophytes and angiosperms, respectively. In this review, we first describe the incidence and anatomical diversity of desiccation-tolerant pteridophytes and discuss recent advances on the origin of DT in vascular plants. Then, we summarize the highly diverse adaptations and mechanisms exhibited by this group and describe how some of these plants could exhibit tolerance to multiple types of abiotic stress. Research on the evolution and regulation of DT in different lineages is crucial to understand how plants have adapted to extreme environments. Thus, in the current scenario of climate change, the knowledge of the whole landscape of DT strategies is of vital importance as a potential basis to improve plant abiotic stress tolerance.
SummaryLonicera macranthoides (LM) and L. japonica (LJ) are medicinal plants widely used in treating viral diseases, such as COVID‐19. Although the two species are morphologically similar, their secondary metabolite profiles are significantly different. Here, metabolomics analysis showed that LM contained ~86.01 mg/g hederagenin‐based saponins, 2000‐fold higher than LJ. To gain molecular insights into its secondary metabolite production, a chromosome‐level genome of LM was constructed, comprising 9 pseudo‐chromosomes with 40 097 protein‐encoding genes. Genome evolution analysis showed that LM and LJ were diverged 1.30–2.27 million years ago (MYA). The two plant species experienced a common whole‐genome duplication event that occurred ∼53.9–55.2 MYA before speciation. Genes involved in hederagenin‐based saponin biosynthesis were arranged in clusters on the chromosomes of LM and they were more highly expressed in LM than in LJ. Among them, oleanolic acid synthase (OAS) and UDP‐glycosyltransferase 73 (UGT73) families were much more highly expressed in LM than in LJ. Specifically, LmOAS1 was identified to effectively catalyse the C‐28 oxidation of β‐Amyrin to form oleanolic acid, the precursor of hederagenin‐based saponin. LmUGT73P1 was identified to catalyse cauloside A to produce α‐hederin. We further identified the key amino acid residues of LmOAS1 and LmUGT73P1 for their enzymatic activities. Additionally, comparing with collinear genes in LJ, LmOAS1 and LmUGT73P1 had an interesting phenomenon of ‘neighbourhood replication’ in LM genome. Collectively, the genomic resource and candidate genes reported here set the foundation to fully reveal the genome evolution of the Lonicera genus and hederagenin‐based saponin biosynthetic pathway.
Due to the importance of Phosphorus (P) on plant development and reproduction, global P security has emerged as a key factor towards global food security. Together with multiple agrochemicals, P-based fertilizers have become the pillars that sustain our food production systems. Therefore, improving the genetics and biology of key crops such as maize, rice, wheat and soybean to develop varieties better adapted to thrive under environments that present low phosphate (Pi) availability and that possess higher Pi-fertilizer use efficiency is imperative. In this review, we summarize the current understanding of Pi nutrition in plants, with particular focus on crops, and provide new perspectives on how to harness the ample repertoire of genetic mechanisms behind plant low-Pi adaptive responses that can be utilized to design smart low-Pi tolerant plants. We discuss on the potential of implementing more integrative, versatile and effective strategies by incorporating genome editing and synthetic biology approaches to reduce Pi-fertilizer input and enable global food security in a more sustainable way.
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