scholarly journals The fungal sesquiterpenoid pyrenophoric acid B uses the plant ABA biosynthetic pathway to inhibit seed germination

2019 ◽  
Author(s):  
Jorge Lozano-Juste ◽  
Marco Masi ◽  
Alessio Cimmino ◽  
Suzette Clement ◽  
Maria A. Fernández ◽  
...  

HighlightThe fungus Pyrenophora semeniperda produces pyrenophoric acid B, a small molecule that exploits the plant ABA biosynthetic pathway to reduce seed germination, increasing its reproductive success.AbstractPyrenophoric acid (P-Acid), P-Acid B and P-Acid C are three phytotoxic sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive weed. When tested in cheatgrass bioassays these metabolites were able to delay seed germination, with P-Acid B being the most active compound. Here, we have investigated the cross-kingdom activity of P-Acid B and its mode of action and found that it activates the ABA signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits seedling establishment in wild-type Arabidopsis thaliana while several mutants affected in the early perception as well as in downstream ABA signaling components were insensitive to the fungal compound. However, in spite of structural similarities between ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose that the fungus Pyrenophora semeniperda manipulates plant ABA biosynthesis as a strategy to reduce seed germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success.

2019 ◽  
Vol 70 (19) ◽  
pp. 5487-5494 ◽  
Author(s):  
Jorge Lozano-Juste ◽  
Marco Masi ◽  
Alessio Cimmino ◽  
Suzette Clement ◽  
Maria A Fernández ◽  
...  

Abstract Pyrenophoric acid (P-Acid), P-Acid B, and P-Acid C are three phytotoxic sesquiterpenoids produced by the ascomycete seed pathogen Pyrenophora semeniperda, a fungus proposed as a mycoherbicide for biocontrol of cheatgrass, an extremely invasive weed. When tested in cheatgrass bioassays, these metabolites were able to delay seed germination, with P-Acid B being the most active compound. Here, we have investigated the cross-kingdom activity of P-Acid B and its mode of action, and found that it activates the abscisic acid (ABA) signaling pathway in order to inhibit seedling establishment. P-Acid B inhibits seedling establishment in wild-type Arabidopsis thaliana, while several mutants affected in the early perception as well as in downstream ABA signaling components were insensitive to the fungal compound. However, in spite of structural similarities between ABA and P-Acid B, the latter is not able to activate the PYR/PYL family of ABA receptors. Instead, we have found that P-Acid B uses the ABA biosynthesis pathway at the level of alcohol dehydrogenase ABA2 to reduce seedling establishment. We propose that the fungus P. semeniperda manipulates plant ABA biosynthesis as a strategy to reduce seed germination, increasing its ability to cause seed mortality and thereby increase its fitness through higher reproductive success.


2020 ◽  
Vol 71 (10) ◽  
pp. 2847-2853 ◽  
Author(s):  
Hiroyuki Nonogaki

Abstract Seed dormancy is induced primarily by abscisic acid (ABA) and maintained through elevated levels of ABA sensitivity in seeds. The core mechanisms of ABA-imposed seed dormancy are emerging, but it is still unclear how these blockages in seeds are eliminated during after-ripening, or what molecular events in imbibed seeds are responsible for the initial stages of germination induction. Some pieces of evidence suggest that a repressor complex, which potentially triggers seed germination through the suppression of ABA signaling components, might be present in seeds. The usual suspect, protein phosphatase 2C, which inactivates kinases and shuts down ABA signaling in the major dormancy pathway, is possibly associated with this complex. Other members, such as WD40 proteins and histone deacetylase subunits, homologs of which are found in the flowering repressor complex, perhaps constitute this complex in seeds. The repressor activity could counteract the dormancy mechanisms in an overwhelming manner, through well-coordinated inactivation and turnover of germination-suppressing transcription factors, which is probably accompanied by chromatin silencing and transcriptional repression of the transcription factor target genes. This review provides a perspective on a putative seed germination-inducing repressor complex, including its possible modes of action and upstream regulators.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Wannarat Pornsiriwong ◽  
Gonzalo M Estavillo ◽  
Kai Xun Chan ◽  
Estee E Tee ◽  
Diep Ganguly ◽  
...  

Organelle-nuclear retrograde signaling regulates gene expression, but its roles in specialized cells and integration with hormonal signaling remain enigmatic. Here we show that the SAL1-PAP (3′-phosphoadenosine 5′- phosphate) retrograde pathway interacts with abscisic acid (ABA) signaling to regulate stomatal closure and seed germination in Arabidopsis. Genetically or exogenously manipulating PAP bypasses the canonical signaling components ABA Insensitive 1 (ABI1) and Open Stomata 1 (OST1); priming an alternative pathway that restores ABA-responsive gene expression, ROS bursts, ion channel function, stomatal closure and drought tolerance in ost1-2. PAP also inhibits wild type and abi1-1 seed germination by enhancing ABA sensitivity. PAP-XRN signaling interacts with ABA, ROS and Ca2+; up-regulating multiple ABA signaling components, including lowly-expressed Calcium Dependent Protein Kinases (CDPKs) capable of activating the anion channel SLAC1. Thus, PAP exhibits many secondary messenger attributes and exemplifies how retrograde signals can have broader roles in hormone signaling, allowing chloroplasts to fine-tune physiological responses.


2014 ◽  
Vol 24 (4) ◽  
pp. 331-339 ◽  
Author(s):  
Andrea Santo ◽  
Efisio Mattana ◽  
Laetitia Hugot ◽  
Paula Spinosi ◽  
Gianluigi Bacchetta

AbstractRouya polygama (Apiaceae) is an endangered Mediterranean species of great phytogeographical and ecological interest, growing on coastal sandy dunes. Intraspecific variability in the responses to constant temperatures (5–25°C) and an alternating temperature regime (25/10°C), salt stress (0–600 mM NaCl) and recovery of seed germination was evaluated among six populations from Sardinia and Corsica. Seeds were non-dormant and germination percentages ranged from 10 to 83%, depending on temperature and population. Differences in germination percentages were mainly due to different seed mortality among seed lots. R. polygama seeds germinated in salt concentrations up to 200 mM NaCl, whereas higher salt concentrations totally inhibited germination. Salt affected seed viability, and the recovery response decreased with increasing salinity and temperature. Inter-population variability and different sensitivity to NaCl in seed germination were detected. Our results are consistent with field germination in a period from autumn to spring, when water is available in the soil and temperatures are not prohibitive for seedling establishment, representing an advantageous ecological adaptation for seedling establishment to the unpredictable Mediterranean rainfall pattern. Further studies on R. polygama are needed to investigate germination requirements at temperatures higher than 25°C and its germination in the field, and to clarify genetic inter-population variability, considering a higher number of populations and possibly extending to North African populations.


2020 ◽  
Vol 13 (9) ◽  
pp. 1284-1297 ◽  
Author(s):  
Zhijuan Wang ◽  
Ziyin Ren ◽  
Chunhong Cheng ◽  
Tao Wang ◽  
Hongtao Ji ◽  
...  

Author(s):  
Jianwen Song ◽  
Lele Shang ◽  
Xin Wang ◽  
Yali Xing ◽  
Wei Xu ◽  
...  

Abstract Seed germination determines when life starts in plants, plays an important role in the efficiency of agricultural production. Nonetheless, our knowledge of the mechanisms that regulate seed germination is limited. Here, we identified a novel gene that encodes mitogen-activated protein kinase 11 (MAPK11), which the expression level in seeds of tomatoes with low germination was significantly higher than that with high germination at room temperature. Overexpression of MAPK11 in TS-9—one accession with the optimum temperature for seed germination at 25 °C—led to a decrease in seed germination, and RNA interference of MAPK11 in TS-34—one accession with the optimum temperature for seed germination at 15 °C—induced increased seed germination at room temperature. Furthermore, we found that lines overexpressing MAPK11 exhibited hypersensitivity to ABA during seed germination. These observations are at least partially explained by our finding that MAPK11 upregulates both NCED1 expression and ABA biosynthesis and that MAPK11 affects ABA signaling and negatively regulates seed germination by influencing the phosphorylation of SnRK2.2 in vivo. In addition, we found that MAPK11 may possibly inhibit SnRK1 activation by binding and phosphorylating SnRK1 in vivo. SnRK1 interacts with ABI5 and suppresses the transcription of ABI5, which contributes to ABA signaling and regulates seed germination in tomato. Thus, our findings demonstrate that in tomato, a mechanism that depends on MAPK11 phosphorylating SnRKs affects ABA signaling and ultimately influences seed germination.


Plants ◽  
2021 ◽  
Vol 10 (11) ◽  
pp. 2437
Author(s):  
Yiru Wang ◽  
Junli Zhang ◽  
Minghao Sun ◽  
Cheng He ◽  
Ke Yu ◽  
...  

Maize vivipary, precocious seed germination on the ear, affects yield and seed quality. The application of multi-omics approaches, such as transcriptomics or metabolomics, to classic vivipary mutants can potentially reveal the underlying mechanism. Seven maize vivipary mutants were selected for transcriptomic and metabolomic analyses. A suite of transporters and transcription factors were found to be upregulated in all mutants, indicating that their functions are required during seed germination. Moreover, vivipary mutants exhibited a uniform expression pattern of genes related to abscisic acid (ABA) biosynthesis, gibberellin (GA) biosynthesis, and ABA core signaling. NCED4 (Zm00001d007876), which is involved in ABA biosynthesis, was markedly downregulated and GA3ox (Zm00001d039634) was upregulated in all vivipary mutants, indicating antagonism between these two phytohormones. The ABA core signaling components (PYL-ABI1-SnRK2-ABI3) were affected in most of the mutants, but the expression of these genes was not significantly different between the vp8 mutant and wild-type seeds. Metabolomics analysis integrated with co-expression network analysis identified unique metabolites, their corresponding pathways, and the gene networks affected by each individual mutation. Collectively, our multi-omics analyses characterized the transcriptional and metabolic landscape during vivipary, providing a valuable resource for improving seed quality.


2021 ◽  
Vol 22 (15) ◽  
pp. 8172
Author(s):  
Orarat Ginsawaeng ◽  
Michal Gorka ◽  
Alexander Erban ◽  
Carolin Heise ◽  
Franziska Brueckner ◽  
...  

During seed germination, desiccation tolerance is lost in the radicle with progressing radicle protrusion and seedling establishment. This process is accompanied by comprehensive changes in the metabolome and proteome. Germination of Arabidopsis seeds was investigated over 72 h with special focus on the heat-stable proteome including late embryogenesis abundant (LEA) proteins together with changes in primary metabolites. Six metabolites in dry seeds known to be important for seed longevity decreased during germination and seedling establishment, while all other metabolites increased simultaneously with activation of growth and development. Thermo-stable proteins were associated with a multitude of biological processes. In the heat-stable proteome, a relatively similar proportion of fully ordered and fully intrinsically disordered proteins (IDP) was discovered. Highly disordered proteins were found to be associated with functional categories development, protein, RNA and stress. As expected, the majority of LEA proteins decreased during germination and seedling establishment. However, four germination-specific dehydrins were identified, not present in dry seeds. A network analysis of proteins, metabolites and amino acids generated during the course of germination revealed a highly connected LEA protein network.


2021 ◽  
Vol 7 (12) ◽  
pp. eabd4113
Author(s):  
Rui Miao ◽  
Wei Yuan ◽  
Yue Wang ◽  
Irene Garcia-Maquilon ◽  
Xiaolin Dang ◽  
...  

The hab1-1abi1-2abi2-2pp2ca-1 quadruple mutant (Qabi2-2) seedlings lacking key negative regulators of ABA signaling, namely, clade A protein phosphatases type 2C (PP2Cs), show more apoplastic H+ efflux in roots and display an enhanced root growth under normal medium or water stress medium compared to the wild type. The presence of low ABA concentration (0.1 micromolar), inhibiting PP2C activity via monomeric ABA receptors, enhances root apoplastic H+ efflux and growth of the wild type, resembling the Qabi2-2 phenotype in normal medium. Qabi2-2 seedlings also demonstrate increased hydrotropism compared to the wild type in obliquely-oriented hydrotropic experimental system, and asymmetric H+ efflux in root elongation zone is crucial for root hydrotropism. Moreover, we reveal that Arabidopsis ABA-insensitive 1, a key PP2C in ABA signaling, interacts directly with the C terminus of Arabidopsis plasma membrane H+-dependent adenosine triphosphatase 2 (AHA2) and dephosphorylates its penultimate threonine residue (Thr947), whose dephosphorylation negatively regulates AHA2.


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