Publications by authors named "Junli Ye"

48 Publications

Downregulated expression of S-RNase attenuates self-incompatibility in "Guiyou No. 1" pummelo.

Hortic Res 2021 Sep 1;8(1):199. Epub 2021 Sep 1.

Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, People's Republic of China.

Self-incompatibility (SI) substantially restricts the yield and quality of citrus. Therefore, breeding and analyzing self-compatible germplasm is of great theoretical and practical significance for citrus. Here, we focus on the mechanism of a self-compatibility mutation in 'Guiyou No. 1' pummelo (Citrus maxima), which is a spontaneous mutant of 'Shatian' pummelo (Citrus maxima, self-incompatibility). The rate of fruit set and the growth of pollen tubes in the pistil confirmed that a spontaneous mutation in the pistil is responsible for the self-compatibility of 'Guiyou No. 1'. Segregation ratios of the S genotype in F progeny, expression analysis, and western blotting validated that the reduced levels of S-RNase mRNA contribute to the loss of SI in 'Guiyou No. 1'. Furthermore, we report a phased assembly of the 'Guiyou No. 1' pummelo genome and obtained two complete and well-annotated S haplotypes. Coupled with an analysis of SV variations, methylation levels, and gene expression, we identified a candidate gene (CgHB40), that may influence the regulation of the S-RNase promoter. Our data provide evidence that a mutation that affects the pistil led to the loss of SI in 'Guiyou No. 1' by influencing a poorly understood mechanism that affects transcriptional regulation. This work significantly advances our understanding of the genetic basis of the SI system in citrus and provides information on the regulation of S-RNase genes.
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http://dx.doi.org/10.1038/s41438-021-00634-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8408199PMC
September 2021

Citrus transcription factor CsHB5 regulates abscisic acid biosynthetic genes and promotes senescence.

Plant J 2021 08 19. Epub 2021 Aug 19.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.

Senescence is a gradual physiological process involving the integration of numerous internal and environmental signals. Abscisic acid (ABA) is a well-known inducer of senescence. However, the regulatory mechanisms underlying ABA-mediated senescence remain largely unknown. Here, we report that the citrus homeodomain leucine zipper I (HD-ZIP I) transcription factor CsHB5 functions as a regulator of ABA-triggered senescence. CsHB5 acts as a nucleus-localized transcriptional activator, the expression of which appeared to be closely associated with citrus senescence. Overexpression of CsHB5 in citrus calli upregulated the expression of ABA- and reactive oxygen species (ROS)-related genes, and significantly increased the content of ABA and hydrogen peroxide (H O ), whereas silencing CsHB5 in citrus calli downregulated the expression of ABA-related genes. Additionally, heterogenous overexpression of CsHB5 in Solanum lycopersicum (tomato) and Arabidopsis thaliana (Arabidopsis) leads to early leaf yellowing under dark-induced senescence conditions. Meanwhile, the levels of ABA and H O in transgenic tomatoes increased significantly and the lycopene content decreased. Transcriptome analysis of CsHB5-overexpressing citrus calli and tomato showed that CsHB5 was involved in multiple senescence-associated processes, including chlorophyll degradation, nutrient compound biosynthesis and transport, as well as ABA and ROS signal transduction. The results of yeast one-hybrid assays, electrophoretic mobility shift assays and dual luciferase assays indicated that CsHB5 directly binds to the promoters of ABA biosynthetic genes, including β-carotene hydroxylase 1 (BCH1) and 9-cis-epoxycarotenoid dioxygenase 2 (NCED2), thereby activating their transcription. Our findings revealed that CsHB5 participates in senescence, at least partly, by directly controlling ABA accumulation. Our work provides insight into the regulatory mechanisms underlying ABA-mediated senescence.
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http://dx.doi.org/10.1111/tpj.15431DOI Listing
August 2021

Lycopene Accumulation in Cara Cara Red-flesh Navel Orange Is Correlated with Weak Abscisic Acid Catabolism.

J Agric Food Chem 2021 Jul 13;69(29):8236-8246. Epub 2021 Jul 13.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry, Huazhong Agricultural University, Wuhan 430070, China.

Lycopene is the main pigment in red-flesh citrus fruits, and its formation is a research hotspot. To explore the basis of lycopene accumulation in red-flesh mutants, we profiled the terpenoid metabolites. Compared with their respective wild types, Cara Cara (Cara) [and Red-Anliu (R-An)] oranges showed increased carotenoid and limonoid aglycone contents and decreased contents of abscisic acid (ABA) catabolites, monoterpenoid volatiles, and sesquiterpenoid volatiles. Cara contained less than half of the amount of ABA glucose ester (ABAGE), the main ABA derivative in oranges. Parallel lower transcript levels of and in Cara were detected at the mature green stage. These results document the changes in terpenoid profiles in Cara and show that the red flesh of citrus color mutants is related to weak ABA catabolism, especially ABAGE, and decreased transcript levels of two genes encoding uridine diphosphate (UDP)-glycosyltransferases that catalyze ABAGE biosynthesis.
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http://dx.doi.org/10.1021/acs.jafc.1c03766DOI Listing
July 2021

Identification of Carbazole Alkaloid Derivatives with Acylhydrazone as Novel Anti-TMV Agents with the Guidance of a Digital Fluorescence Visual Screening.

J Agric Food Chem 2021 Jul 24;69(26):7458-7466. Epub 2021 Jun 24.

State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, Hubei 430070, P. R. China.

Difficulty in preventing crops from plant viruses urges to discover novel efficient antiviral chemicals, which is sped up by precise screening methods. Fluorescence-based methods have recently been applied as innovative and rapid tools for visually monitoring the replication of viruses and screening of antivirals, whereas the quantification of fluorescence signals mainly depends on manually calculating the fluorescent spots, which is time-consuming and imprecise. In the present work, the fluorescence spots were automatically identified, and the fluorescence area was directly quantified by a program developed in our group, which avoided subjective errors from the operators. We further employed this digital and visual screening assay to identify antivirals using the tobacco mosaic virus-green fluorescence protein (TMV-GFP) construct, in which the expression of GFP intuitively reflected the efficacy of antivirals. The accuracy of this assay was validated by quantifying the activities of the commercial antiviral inhibitors ribavirin and ningnanmycin and then was applied to evaluate the subtle activity differences of a series of newly synthesized carbazole and β-carboline alkaloid derivatives. Among them, compounds (76%) and (63%) exhibited anti-TMV activities comparable to that of ningnanmycin (65%) at 50 μM, and they delayed the multiplication of TMV in the early stage of infection without phytotoxicity. Taken together, these findings demonstrated that the digital and visual TMV-GFP screening method was competent to test the antiviral activities of compounds with subtle modifications and facilitated the discovery of novel antivirals.
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http://dx.doi.org/10.1021/acs.jafc.1c00897DOI Listing
July 2021

Using high-throughput multiple optical phenotyping to decipher the genetic architecture of maize drought tolerance.

Genome Biol 2021 06 24;22(1):185. Epub 2021 Jun 24.

National Key Laboratory of Crop Genetic Improvement, National Center of Plant Gene Research, and Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan, 430070, China.

Background: Drought threatens the food supply of the world population. Dissecting the dynamic responses of plants to drought will be beneficial for breeding drought-tolerant crops, as the genetic controls of these responses remain largely unknown.

Results: Here we develop a high-throughput multiple optical phenotyping system to noninvasively phenotype 368 maize genotypes with or without drought stress over a course of 98 days, and collected multiple optical images, including color camera scanning, hyperspectral imaging, and X-ray computed tomography images. We develop high-throughput analysis pipelines to extract image-based traits (i-traits). Of these i-traits, 10,080 were effective and heritable indicators of maize external and internal drought responses. An i-trait-based genome-wide association study reveals 4322 significant locus-trait associations, representing 1529 quantitative trait loci (QTLs) and 2318 candidate genes, many that co-localize with previously reported maize drought responsive QTLs. Expression QTL (eQTL) analysis uncovers many local and distant regulatory variants that control the expression of the candidate genes. We use genetic mutation analysis to validate two new genes, ZmcPGM2 and ZmFAB1A, which regulate i-traits and drought tolerance. Moreover, the value of the candidate genes as drought-tolerant genetic markers is revealed by genome selection analysis, and 15 i-traits are identified as potential markers for maize drought tolerance breeding.

Conclusion: Our study demonstrates that combining high-throughput multiple optical phenotyping and GWAS is a novel and effective approach to dissect the genetic architecture of complex traits and clone drought-tolerance associated genes.
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http://dx.doi.org/10.1186/s13059-021-02377-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8223302PMC
June 2021

Curcumin relieves mice gastric emptying dysfunction induced by L-arginine and atropine through interstitial cells of Cajal.

Exp Ther Med 2021 Jun 24;21(6):548. Epub 2021 Mar 24.

Department of Physiology and Pathophysiology, School of Basic Medicine, Qingdao University, Qingdao, Shandong 266021, P.R. China.

Curcumin is natural polyphenol from rhizomes with several biological properties. Our previous studies demonstrated that curcumin inhibited functional gastric emptying disorders induced by L-arginine, the precursor of nitric oxide (NO), and atropine, an acetylcholine receptor (AChR) blocker. However, the mechanism of action of curcumin remains unclear. In the present study, mouse models of functional gastric emptying disorders induced by L-arginine and atropine were used to examine changes in interstitial cells of Cajal (ICC) and NO- and ACh-mediated regulation of gastrointestinal motility. Curcumin pre-treatment ameliorated the gastric emptying rate in mice treated with L-arginine or atropine (P<0.01). NO content and NO synthase activity significantly increased in the stomachs of L-arginine-treated mice, compared with controls (P<0.01). Acetylcholinesterase activity (P<0.01) and mRNA expression (P<0.01), as well as AChR mRNA levels (P<0.05) significantly decreased following atropine treatment. Moreover, in both models, the levels of c-kit, anoctamin 1 and connexin 43 significantly decreased in the stomach (P<0.01). Conversely, curcumin pre-treatment inhibited the changes induced by L-arginine and atropine (P<0.01 or P<0.05). By affecting the production of exogenous NO, the effects of Ach-AchR and the biomarkers of ICC, curcumin relieves the gastric emptying dysfunction in mice.
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http://dx.doi.org/10.3892/etm.2021.9980DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8027730PMC
June 2021

Multiomics-based dissection of citrus flavonoid metabolism using a Citrus reticulata × Poncirus trifoliata population.

Hortic Res 2021 Mar 1;8(1):56. Epub 2021 Mar 1.

Key Laboratory of Horticultural Plant Biology, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, 430070, China.

Deciphering the genetic basis of plant secondary metabolism will provide useful insights for genetic improvement and enhance our fundamental understanding of plant biological processes. Although citrus plants are among the most important fruit crops worldwide, the genetic basis of secondary metabolism in these plants is largely unknown. Here, we use a high-density linkage map to dissect large-scale flavonoid metabolic traits measured in different tissues (young leaf, old leaf, mature pericarp, and mature pulp) of an F pseudo-testcross citrus population. We detected 80 flavonoids in this population and identified 138 quantitative trait loci (QTLs) for 57 flavonoids in these four tissues. Based on transcriptional profiling and functional annotation, twenty-one candidate genes were identified, and one gene encoding flavanone 3-hydroxylase (F3H) was functionally verified to result in naturally occurring variation in dihydrokaempferol content through genetic variations in its promoter and coding regions. The abundant data resources collected for diverse citrus germplasms here lay the foundation for complete characterization of the citrus flavonoid biosynthetic pathway and will thereby promote efficient utilization of metabolites in citrus quality improvement.
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http://dx.doi.org/10.1038/s41438-021-00472-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7917093PMC
March 2021

Ethylene activation of carotenoid biosynthesis by a novel transcription factor CsERF061.

J Exp Bot 2021 04;72(8):3137-3154

Key Laboratory of Horticultural Plant Biology of MOE (Ministry of Education), Huazhong Agricultural University, Wuhan, Hubei, China.

Chromoplast-specific lycopene β-cyclase (LCYb2) is a critical carotenogenic enzyme, which controls the massive accumulation of downstream carotenoids, especially provitamin A carotenoids, in citrus. Its regulatory metabolism is largely unknown. Here, we identified a group I ethylene response factor, CsERF061, in citrus by yeast one-hybrid screen with the promoter of LCYb2. The expression of CsERF061 was induced by ethylene. Transcript and protein levels of CsERF061 were increased during fruit development and coloration. CsERF061 is a nucleus-localized transcriptional activator, which directly binds to the promoter of LCYb2 and activates its expression. Overexpression of CsERF061 in citrus calli and tomato fruits enhanced carotenoid accumulation by increasing the expression of key carotenoid pathway genes, and increased the number of chromoplasts needed to sequester the elevated concentrations of carotenoids, which was accompanied by changes in the concentrations of abscisic acid and gibberellin. Electrophoretic mobility shift and dual-luciferase assays verified that CsERF061 activates the promoters of nine other key carotenoid pathway genes, PSY1, PDS, CRTISO, LCYb1, BCH, ZEP, NCED3, CCD1, and CCD4, revealing the multitargeted regulation of CsERF061. Collectively, our findings decipher a novel regulatory network of carotenoid enhancement by CsERF061, induced by ethylene, which will be useful for manipulating carotenoid accumulation in citrus and other plants.
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http://dx.doi.org/10.1093/jxb/erab047DOI Listing
April 2021

A fruit ripening-associated transcription factor CsMADS5 positively regulates carotenoid biosynthesis in citrus.

J Exp Bot 2021 04;72(8):3028-3043

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China.

Carotenoids in citrus contribute to the quality of the fruit, but the mechanism of its transcriptional regulation is fairly unknown. Here, we characterized a citrus FRUITFULL sub-clade MADS gene, CsMADS5, that was ripening-inducible and acted as a nucleus-localized trans-activator. Transient overexpression of CsMADS5 in citrus induced fruit coloration and enhanced carotenoid concentrations. The expression of carotenogenic genes including phytoene synthase (PSY), phytoene desaturase (PDS), and lycopene β-cyclase 1 (LCYb1) was increased in the peels of fruits overexpressing CsMADS5. Similar results were observed from stable overexpression of CsMADS5 in tomato fruits and citrus calli, even though the effect of CsMADS5 on carotenoid metabolism in transgenic citrus calli was limited. Further biochemical analyses demonstrated that CsMADS5 activated the transcription of PSY, PDS, and LCYb1 by directly binding to their promoters. We concluded that CsMADS5 positively regulates carotenoid biosynthesis in fruits by directly activating the transcription of carotenogenic genes. Moreover, CsMADS5 physically interacted with a positive regulator CsMADS6, indicating that CsMADS5 may form an enhancer complex with CsMADS6 to synergistically promote carotenoid accumulation. These findings expand our understanding of the complex transcriptional regulatory hierarchy of carotenoid biosynthesis during fruit ripening.
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http://dx.doi.org/10.1093/jxb/erab045DOI Listing
April 2021

A Citrus Phosphate Starvation Response Factor CsPHL3 Negatively Regulates Carotenoid Metabolism.

Plant Cell Physiol 2021 Jul;62(3):482-493

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China.

Carotenoids provide precursors for the biosynthesis of strigolactones, which are a new class of hormones that are essential in phosphate (Pi) signaling during plant development. Carotenoid metabolism is a finely tuned pathway, but our understanding of the regulation mechanisms is still limited. In this study, we isolated a protein designated as CsPHL3 from citrus. CsPHL3 belonged to the Pi starvation response factor (PHR)-like subclade and was upregulated by low Pi. Acting as a nucleus-localized protein with transactivation activity, CsPHL3 bound directly to activate the promoter of a key metabolic gene, lycopene β-cyclase1 (LCYb1). Transgenic analysis revealed that the CsPHL3-overexpressing tomato plants exhibited abnormal growth, like the plants grew under limited Pi conditions. The transgenic lines showed reduced carotenoid contents and elevated expression of LCYb genes but downregulation of other key carotenogenic genes, including phytoene synthase (PSY). Moreover, CsPHL3 induced anthocyanin biosynthesis and affected Pi signaling in the transgenic plants. We further demonstrated that the expression of PSY was negatively regulated by CsPHL3 and high Pi. It is concluded that CsPHL3 is a Pi starvation response factor that negatively regulates carotenoid metabolism by modulating the expression of carotenogenic genes. Establishment of the CsPHL3-CsLCYb1 network provides new valuable knowledge of the function and underlying mechanism of PHR transcription factors and expands our understanding of the complex regulation mechanisms of carotenoid biosynthesis.
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http://dx.doi.org/10.1093/pcp/pcab007DOI Listing
July 2021

Building the Synthetic Biology Toolbox with Enzyme Variants to Expand Opportunities for Biofortification of Provitamin A and Other Health-Promoting Carotenoids.

J Agric Food Chem 2020 Oct 19;68(43):12048-12057. Epub 2020 Oct 19.

Key Laboratory of Horticultural Plant Biology of MOE (Ministry of Education), Huazhong Agricultural University, Wuhan, Hubei 430070, China.

Carotenoids are a large class of structures that are important in human health and include both provitamin A and nonprovitamin A compounds. Vitamin A deficiency is a global health problem that can be alleviated by enriching provitamin A carotenoids in a range of food crops. Suitable plants for biofortification are those with high levels of the provitamin A biosynthetic precursor, lycopene, which is enzymatically converted by lycopene β-cyclase (LCYB) to β-carotene, a provitamin A carotenoid. Crops, such as citrus, naturally accumulate high levels of provitamin A and other health-promoting carotenoids. Such plants may have useful genes to expand the synthetic biology toolbox for producing a range of phenotypes, including both high provitamin A crops and crops with unique compositions of health-promoting carotenoids. To examine enzyme variants having different activity levels, we introduced two citrus LCYB alleles into tomato, a plant with fruit rich in lycopene. Overexpression in tomato of the stronger allele of the citrus chromoplast-specific lycopene β-cyclase () produced "golden" transgenic tomato fruits with 9.3-fold increased levels of β-carotene at up to 1.5 mg/g dry weight. The use of the weaker allele, , also led to enhanced levels of β-carotene but in the context of a more heterogeneous composition of carotenoids. From a synthetic biology standpoint, these allelic differences have value for producing cultivars with unique carotenoid profiles. Overexpression of the citrus genes was accompanied by increased expression of other genes encoding carotenoid biosynthetic enzymes and increased size and number of chromoplasts needed to sequester the elevated levels of carotenoids in the transgenic tomato fruits. The overexpression of the citrus genes also led to a pleiotropic effect on profiles of phytohormones and primary metabolites. Our findings show that enzyme variants are essential synthetic biology parts needed to create a wider range of metabolic engineering products. In this case, strong and weak variants of LCYB proved useful in creating dietary sources to alleviate vitamin A deficiency or, alternatively, to create crops with a heterogeneous composition including provitamin A and healthful, nonprovitamin A carotenoids.
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http://dx.doi.org/10.1021/acs.jafc.0c04740DOI Listing
October 2020

The effect of β-cyclocitral treatment on the carotenoid content of transgenic Marsh grapefruit (Citrus paradisi Macf.) suspension-cultured cells.

Phytochemistry 2020 Dec 20;180:112509. Epub 2020 Sep 20.

School of Biological Sciences, Royal Holloway, University of London, Egham Hill, Egham, Surrey, TW20 0EX, UK. Electronic address:

This work reports the development of suspension culture system of transgenic Marsh grapefruit (Citrus paradisi Macf., Rutaceae) callus overexpressing bacterial phytoene synthase; and the use of this suspension culture to investigate the effects of β-cyclocitral on carotenoid content and composition. At a β-cyclocitral concentration of 0.5 mM and after ten days cultivation, analysis of the carotenoids showed a significant increase in the content of β-, α-carotene, and phytoene predominantly. The maximal increase in total provitamin A carotenoids content following β-cyclocitral application was ~2-fold higher than the control, reaching 245.8 μg/g DW. The trend for increased transcript levels of biosynthetic genes PSY and ZDS correlated with the enhancement of the content of these carotenes following β-cyclocitral treatment and GC-MS based metabolite profiling showed significant changes of metabolite levels across intermediary metabolism. These findings suggest that β-cyclocitral can act as a chemical elicitor, to enhance the formation of carotenes in citrus suspension-cultured cells (SCC), which could be utilized in studying the regulation of carotenoid biosynthesis and biotechnological application to the renewable production of nutritional carotenoids.
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http://dx.doi.org/10.1016/j.phytochem.2020.112509DOI Listing
December 2020

Curcumin Alleviates the Side Effects of Cisplatin on Gastric Emptying of Mice by Inhibiting the Signal Changes of Acetylcholine and Interstitial Cells of Cajal.

J Med Food 2020 Sep 20;23(9):920-927. Epub 2020 Aug 20.

Department of Physiology and Pathophysiology, Qingdao University Medical College, Qingdao, P.R. China.

Cisplatin is a widely used anticancer drug that has adverse effects on gastrointestinal function. Curcumin is a natural polyphenol extracted from the rhizome of turmeric that has a wide range of biological activities. The present study investigated the effects of cisplatin on gastric emptying in mice and examined whether these can be inhibited by curcumin. We found that pretreatment with curcumin (200 mg/kg/day) for 10-30 days partly inhibited the decreases in gastric emptying rate and body weight induced by cisplatin. Furthermore, cisplatin reduced acetylcholine (ACh) concentration and the messenger RNA (mRNA) level of ACh receptor (AChR) as well as acetylcholinesterase activity in the stomach of mice; caused ultrastructural damage to interstitial cells of Cajal (ICC); and altered the expression of c-kit/stem cell factor and the gap junction protein connexin 43 in ICC. Curcumin pretreatment inhibited the effects of cisplatin on ACh indicators and ICC. These results demonstrate that curcumin can protect against cisplatin-induced gastric emptying disorder and thus has therapeutic potential for alleviating this condition in cancer patients receiving cisplatin chemotherapy.
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http://dx.doi.org/10.1089/jmf.2019.4599DOI Listing
September 2020

A NAC transcription factor and its interaction protein hinder abscisic acid biosynthesis by synergistically repressing NCED5 in Citrus reticulata.

J Exp Bot 2020 06;71(12):3613-3625

National R&D Center for Citrus Preservation, Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan, P.R. China.

Although abscisic acid (ABA) is a vital regulator of fruit ripening and several transcription factors have been reported to regulate ABA biosynthesis, reports of the effect of ABA on citrus ripening and the regulation of its biosynthesis by a multiple-transcription-factor complex are scarce. In the present study, a systematic metabolic, cytological, and transcriptome analysis of an ABA-deficient mutant (MT) of Citrus reticulata cv. Suavissima confirmed the positive effect of ABA on the citrus ripening process. The analysis of transcriptome profiles indicated that CrNAC036 played an important role in the ABA deficiency of the mutant, most likely due to an effect on the expression of 9-cis-epoxycarotenoid dioxygenase 5 (CrNCED5). Electrophoretic mobility shift assays and dual luciferase assays demonstrated that CrNAC036 can directly bind and negatively regulate CrNCED5 expression. Furthermore, yeast two-hybrid, bimolecular fluorescence complementation, and dual luciferase assays demonstrated that CrNAC036 interacted with CrMYB68, also down-regulating the expression of CrNCED5. Taken together, our results suggest that CrNAC036 and CrMYB68 synergistically inhibit ABA biosynthesis in citrus fruit by regulating the expression of CrNCED5.
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http://dx.doi.org/10.1093/jxb/eraa118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7475259PMC
June 2020

Evolution of self-compatibility by a mutant S-RNase in citrus.

Nat Plants 2020 02 13;6(2):131-142. Epub 2020 Feb 13.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, P. R. China.

Self-incompatibility (SI) is an important mechanism that prevents self-fertilization and inbreeding in flowering plants. The most widespread SI system utilizes S ribonucleases (S-RNases) and S-locus F-boxes (SLFs) as S determinants. In citrus, SI is ancestral, and Citrus maxima (pummelo) is self-incompatible, while Citrus reticulata (mandarin) and its hybrids are self-compatible (SC). Here, we identify nine highly polymorphic pistil-specific, developmentally expressed S-RNases from pummelo that segregate with S haplotypes in a gametophytic manner and cluster with authentic S-RNases. We provide evidence that these S-RNases function as the female S determinants in citrus. Moreover, we show that each S-RNase is linked to approximately nine SLFs. In an analysis of 117 citrus SLF and SFL-like (SLFL) genes, we reveal that they cluster into 12 types and that the S-RNases and intra-haplotypic SLF and SLFL genes co-evolved. Our data support the notion that citrus have a S locus comprising a S-RNase and several SLFs that fit the non-self-recognition model. We identify a predominant single nucleotide mutation, S-RNase, in SC citrus, which provides a 'natural' loss of function. We show that SI-SC transitions due to the S-RNase initially arose in mandarin, spreading to its hybrids and became fixed. Identification of an evolutionarily distant new genus utilizing the S-RNase-based SI system, >100 million years separated from the nearest S-RNase family, is a milestone for evolutionary comparative studies.
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http://dx.doi.org/10.1038/s41477-020-0597-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7030955PMC
February 2020

MRI Combined with Magnetic Resonance Cholangiopancreatography for Diagnosis of Benign and Malignant Pancreatic Intraductal Papillary Mucinous Neoplasms.

Curr Med Imaging Rev 2019 ;15(5):504-510

Department of Pathophysiology, Medical College, Qingdao University, Qingdao, Shandong 266071, China.

Background: Intraductal papillary mucinous neoplasms (IPMNs) are among the important premalignant lesions. Early detection and intervention are critical to positive patient outcomes. Magnetic resonance imaging (MRI) can be used to evaluate the malignancy of IPMNs, and magnetic resonance cholangiopancreatography (MRCP) is recommended for follow-up of pancreatic cystic lesions.

Objective: To evaluate the diagnostic performance of MRI combined with MRCP in determining the malignant potential of pancreas IPMN.

Methods: This is a retrospective study of 55 patients with 58 pancreatic lesions confirmed after surgery, which were analyzed and divided into two groups, a benign IPMN group (n = 27) and a malignant IPMN group (n = 31). Two radiologists analyzed the high-risk stigmata and worrisome features of pancreas IPMN to evaluate the malignant potential. Score all the lesions as proposed by the international consensus guidelines 2012, and calculate the sensitivity, specificity and accuracy.

Results: There were significant differences of size, enhancement of solid components, and degree of dilation of the main pancreatic duct between benign and malignant IPMN (P < 0.05). However, differences in gender, age and location of disease between the two groups were not statistically significant (P > 0.05). The sensitivity, specificity and accuracy of MRI combined with MRCP in preoperative diagnosis of malignant IPMNs were 90.3% (28/31), 70.4% (19/27) and 81.0% (47/58) respectively, when at least one worrisome feature was present.

Conclusion: MRI combined with MRCP is useful in the evaluation of the benign and malignant pancreas IPMN.
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http://dx.doi.org/10.2174/1573405614666180807113422DOI Listing
October 2020

Citrus PH4-Noemi regulatory complex is involved in proanthocyanidin biosynthesis via a positive feedback loop.

J Exp Bot 2020 02;71(4):1306-1321

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China.

Proanthocyanidins (PAs; or condensed tannins) are a major class of flavonoids that contribute to citrus fruit quality. However, the molecular mechanism responsible for PA biosynthesis and accumulation in citrus remains unclear. Here, we identify a PH4-Noemi regulatory complex that regulates proanthocyanidin biosynthesis in citrus. Overexpression of PH4 or Noemi in citrus calli activated the expression of PA biosynthetic genes and significantly increased the PA content. Interestingly, Noemi was also shown to be up-regulated in CsPH4-overexpressing lines compared with wild-type calli. Simultaneously, CsPH4 partially complemented the PA-deficient phenotype of the Arabidopsis tt2 mutant and promoted PA accumulation in the wild-type. Further analysis revealed that CsPH4 interacted with Noemi, and together these proteins synergistically activated the expression of PA biosynthetic genes by directly binding to the MYB-recognizing elements (MRE) of the promoters of these genes. Moreover, CsPH4 could directly bind to the promoter of Noemi and up-regulate the expression of this gene. These findings explain how the CsPH4-Noemi regulatory complex contributes to the activation of PA biosynthetic genes via a positive feedback loop and provide new insights into the molecular mechanisms underlying PA biosynthesis, which can be effectively employed for metabolic engineering to improve citrus fruit quality.
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http://dx.doi.org/10.1093/jxb/erz506DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7031078PMC
February 2020

Natural Variation in CCD4 Promoter Underpins Species-Specific Evolution of Red Coloration in Citrus Peel.

Mol Plant 2019 09 16;12(9):1294-1307. Epub 2019 May 16.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China. Electronic address:

Carotenoids and apocarotenoids act as phytohormones and volatile precursors that influence plant development and confer aesthetic and nutritional value critical to consumer preference. Citrus fruits display considerable natural variation in carotenoid and apocarotenoid pigments. In this study, using an integrated genetic approach we revealed that a 5' cis-regulatory change at CCD4b encoding CAROTENOID CLEAVAGE DIOXYGENASE 4b is a major genetic determinant of natural variation in C apocarotenoids responsible for red coloration of citrus peel. Functional analyses demonstrated that in addition the known role in synthesizing β-citraurin, CCD4b is also responsible for the production of another important C apocarotenoid pigment, β-citraurinene. Furthermore, analyses of the CCD4b promoter and transcripts from various citrus germplasm accessions established a tight correlation between the presence of a putative 5' cis-regulatory enhancer within an MITE transposon and the enhanced allelic expression of CCD4b in C apocarotenoid-rich red-peeled accessions. Phylogenetic analysis provided further evidence that functional diversification of CCD4b and naturally occurring variation of the CCD4b promoter resulted in the stepwise evolution of red peels in mandarins and their hybrids. Taken together, our findings provide new insights into the genetic and evolutionary basis of apocarotenoid diversity in plants, and would facilitate breeding efforts that aim to improve the nutritional and aesthetic value of citrus and perhaps other fruit crops.
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http://dx.doi.org/10.1016/j.molp.2019.04.014DOI Listing
September 2019

Genome sequencing and CRISPR/Cas9 gene editing of an early flowering Mini-Citrus (Fortunella hindsii).

Plant Biotechnol J 2019 11 21;17(11):2199-2210. Epub 2019 May 21.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, Wuhan, China.

Hongkong kumquat (Fortunella hindsii) is a wild citrus species characterized by dwarf plant height and early flowering. Here, we identified the monoembryonic F. hindsii (designated as 'Mini-Citrus') for the first time and constructed its selfing lines. This germplasm constitutes an ideal model for the genetic and functional genomics studies of citrus, which have been severely hindered by the long juvenility and inherent apomixes of citrus. F. hindsii showed a very short juvenile period (~8 months) and stable monoembryonic phenotype under cultivation. We report the first de novo assembled 373.6 Mb genome sequences (Contig-N50 2.2 Mb and Scaffold-N50 5.2 Mb) for F. hindsii. In total, 32 257 protein-coding genes were annotated, 96.9% of which had homologues in other eight Citrinae species. The phylogenomic analysis revealed a close relationship of F. hindsii with cultivated citrus varieties, especially with mandarin. Furthermore, the CRISPR/Cas9 system was demonstrated to be an efficient strategy to generate target mutagenesis on F. hindsii. The modifications of target genes in the CRISPR-modified F. hindsii were predominantly 1-bp insertions or small deletions. This genetic transformation system based on F. hindsii could shorten the whole process from explant to T mutant to about 15 months. Overall, due to its short juvenility, monoembryony, close genetic background to cultivated citrus and applicability of CRISPR, F. hindsii shows unprecedented potentials to be used as a model species for citrus research.
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http://dx.doi.org/10.1111/pbi.13132DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6790359PMC
November 2019

SLAF-Based Construction of a High-Density Genetic Map and Its Application in QTL Mapping of Carotenoids Content in Citrus Fruit.

J Agric Food Chem 2019 Jan 10;67(3):994-1002. Epub 2019 Jan 10.

Key Laboratory of Horticultural Plant Biology (Ministry of Education) , Huazhong Agricultural University , Wuhan , China.

Carotenoids are important antioxidant components in the human diet. To develop carotenoid-rich agricultural products by genetic intervention, understanding the genetic basis of carotenoids variation is essential. In this study, we constructed a high-density integrated genetic map with 3817 molecular markers using specific locus amplified fragment (SLAF) sequencing from a C. reticulata × P. trifoliata F pseudotestcross population. A total of 17 significant quantitative trait loci (QTLs) distributed on Chromosomes (Chr) 2, 3, 5, 6, and 9 were detected to determine the carotenoid variation in the population. In particular, three QTL colocalizations for multiple carotenoid constituents were observed on Chr 2, 3, and 9, one of which was located on Chr2:34,654,608-35430715 accounted for 20.1-25.4% of the variation of luteoxanthin, auroxanthin, lutein, violaxanthin, and total carotenoid content. Overall, this study provides a genetic foundation for marker-assisted selection (MAS) breeding of nutritionally enhanced citrus fruit.
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http://dx.doi.org/10.1021/acs.jafc.8b05176DOI Listing
January 2019

Combining high-throughput micro-CT-RGB phenotyping and genome-wide association study to dissect the genetic architecture of tiller growth in rice.

J Exp Bot 2019 01;70(2):545-561

National Key Laboratory of Crop Genetic Improvement and National Center of Plant Gene Research, Agricultural Bioinformatics Key Laboratory of Hubei Province, College of Informatics, and College of Engineering, Huazhong Agricultural University, Wuhan, China.

Manual phenotyping of rice tillers is time consuming and labor intensive, and lags behind the rapid development of rice functional genomics. Thus, automated, non-destructive methods of phenotyping rice tiller traits at a high spatial resolution and high throughput for large-scale assessment of rice accessions are urgently needed. In this study, we developed a high-throughput micro-CT-RGB imaging system to non-destructively extract 739 traits from 234 rice accessions at nine time points. We could explain 30% of the grain yield variance from two tiller traits assessed in the early growth stages. A total of 402 significantly associated loci were identified by genome-wide association study, and dynamic and static genetic components were found across the nine time points. A major locus associated with tiller angle was detected at time point 9, which contained a major gene, TAC1. Significant variants associated with tiller angle were enriched in the 3'-untranslated region of TAC1. Three haplotypes for the gene were found, and rice accessions containing haplotype H3 displayed much smaller tiller angles. Further, we found two loci containing associations with both vigor-related traits identified by high-throughput micro-CT-RGB imaging and yield. The superior alleles would be beneficial for breeding for high yield and dense planting.
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http://dx.doi.org/10.1093/jxb/ery373DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6322582PMC
January 2019

The Citrus Transcription Factor CsMADS6 Modulates Carotenoid Metabolism by Directly Regulating Carotenogenic Genes.

Plant Physiol 2018 04 20;176(4):2657-2676. Epub 2018 Feb 20.

Key Laboratory of Horticultural Plant Biology (Ministry of Education), Huazhong Agricultural University, 430070 Wuhan, China

Although remarkable progress has been made toward understanding carotenoid biosynthesis, the mechanisms that regulate the transcription of carotenogenic genes remain poorly understood. Lycopene β-cyclases (LCYb) are critical enzymes located at the branch point of the carotenoid biosynthetic pathway. Here, we used the promoter sequence of as bait in a yeast one-hybrid screen for promoter-binding proteins from sweet orange (). This screen identified a MADS transcription factor, CsMADS6, that was coordinately expressed with fruit development and coloration. Acting as a nucleus-localized transcriptional activator, CsMADS6 directly bound the promoter of and activated its expression. Overexpression of in citrus calli increased carotenoid contents and induced the expression of and other carotenogenic genes, including (), (), and (). CsMADS6 up-regulated the expression of , , and by directly binding to their promoters, which suggested the multitargeted regulation of carotenoid metabolism by CsMADS6. In addition, the ectopic expression of in tomato () affected carotenoid contents and the expression of carotenogenic genes. The sepals of -overexpressing tomato lines exhibited dramatic changes in carotenoid profiles, accompanied by changes in plastid ultrastructure. Global transcriptome analysis of transgenic sepals revealed that CsMADS6 regulates a series of pathways that promote increases in flux through the carotenoid pathway. Overall, these findings establish that CsMADS6 directly regulates and other carotenogenic genes to coordinately and positively modulate carotenoid metabolism in plants, which may provide strategies to improve the nutritional quality of crops.
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http://dx.doi.org/10.1104/pp.17.01830DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5884614PMC
April 2018

A comprehensive proteomic analysis of elaioplasts from citrus fruits reveals insights into elaioplast biogenesis and function.

Hortic Res 2018 7;5. Epub 2018 Feb 7.

1Key Laboratory of Horticultural Plant Biology (Ministry of Education), College of Horticulture and Forestry Science, Huazhong Agricultural University, Wuhan, 430070 China.

Elaioplasts of citrus peel are colorless plastids which accumulate significant amounts of terpenes. However, other functions of elaioplasts have not been fully characterized to date. Here, a LC-MS/MS shotgun technology was applied to identify the proteins from elaioplasts that were highly purified from young fruit peel of kumquat. A total of 655 putative plastid proteins were identified from elaioplasts according to sequence homology and manual curation. Based on functional classification via Mapman, ~50% of the identified proteins fall into six categories, including protein metabolism, transport, and lipid metabolism. Of note, elaioplasts contained ATP synthase and ADP, ATP carrier proteins at high abundance, indicating important roles for ATP generation and transport in elaioplast biogenesis. Additionally, a comparison of proteins between citrus chromoplast and elaioplast proteomes suggest a high level of functional conservation. However, some distinctive protein profiles were also observed in both types of plastids notably for isoprene biosynthesis in elaioplasts, and carotenoid metabolism in chromoplasts. In conclusion, this comprehensive proteomic study provides new insights into the major metabolic pathways and unique characteristics of elaioplasts and chromoplasts in citrus fruit.
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http://dx.doi.org/10.1038/s41438-017-0014-xDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5802726PMC
February 2018

Data on water consumption in streptozotocin-induced diabetic mice by a novel peach gum-derived polysaccharide.

Data Brief 2017 Jun 23;12:358-360. Epub 2017 Apr 23.

Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.

The data presented in this article are related to the article entitled "The impact of a novel peach gum-derived polysaccharide on postprandial blood glucose control in streptozotocin-induced diabetic mice" (Wang et al., 2017) [1]. Polydipsia was one of the most important symptoms of diabetic mellitus (DM) mice, which showed more water consumption than normal ones. The water consumption of DM mice in different groups administrated with metformin hydrochloride or a novel polysaccharide (coded as PGPSD) were exhibited in this article (Fig. 1). The field data set is made publicly available to enable critical or extended analyzes.
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http://dx.doi.org/10.1016/j.dib.2017.04.022DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5412007PMC
June 2017

The role of autophagy in pro-inflammatory responses of microglia activation via mitochondrial reactive oxygen species in vitro.

J Neurochem 2017 07 18;142(2):215-230. Epub 2017 May 18.

Department of Clinical Laboratory, the Affiliated Hospital of Medical College Qingdao University, Qingdao, China.

Microglia over-activation contributes to neurodegenerative processes by neurotoxin factors and pro-inflammatory molecules of pro-inflammatory processes. Mitochondrial reactive oxygen species (ROS) and autophagy pathway might be involved in microglial activation, but the underlying mechanism is unclear. Here, we regulated autophagy pathway of microglia in vitro by autophagy inhibition (3-methyladenine treatment, siRNA-Beclin 1 or siRNA-ATG5 transfection) or induction (rapamycin treatment) in murine microglial BV-2 cells or cultured primary mouse microglial cells. And we found that autophagy inhibition could sensitize mitochondrial profile and microglial activation of cultured microglial cells, demonstrated by significant production of mitochondrial ROS, loss of mitochondrial membrane potential, secretion of pro-inflammatory cytokines including interleukin 1β (IL-1β), interleukin 6 (IL-6), interleukin 12 (IL-12) and tumor necrosis factor α and marked activation of mitogen-activated proteinkinases (MAPKs) and nuclear factor κB (NF-κB). These effects could be blocked by specific inhibitors of MAPK and NF-κB or mitochondrial antioxidants, Mito-TEMPO. Meanwhile, induction of autophagy with rapamycin treatment could significantly suppress microglial inflammatory responses, mitochondrial ROS production, activation of MAPKs and NF-κB. Taken together, our in vitro results from primary cultured microglia and BV-2 cell lines indicated that autophagy inhibition might participate in brain macrophage or microglia over-activation and mitochondrial ROS generation might be involved in the regulatory microglial pro-inflammatory responses.
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http://dx.doi.org/10.1111/jnc.14042DOI Listing
July 2017

The impact of a novel peach gum-derived polysaccharide on postprandial blood glucose control in streptozotocin-induced diabetic mice.

Int J Biol Macromol 2017 May 20;98:379-386. Epub 2017 Jan 20.

Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University, Wuhan 430070, China.

Peach [Prunus persica (L.)] gum exudates are produced by the trunks and fruits in peach gummosis. Clinically, these exudates have been used to treat diabetes in China, though the molecular mechanism underlying remains unclear. In the current study, a novel peach gum-derived polysaccharide was isolated, designated as PGPSD, and its anti-diabetic effect was assessed in mice. This polysaccharide was composed of arabinose, xylose and galactose in the molar ratio of 5.98:1:3.55, with the average molecular weight at 1.00×10Da. The animal study demonstrated that the PGPSD polysaccharide significantly lowered the postprandial blood glucose in streptozotocin-induced diabetic mice. Histology and immunohistochemistry results further confirmed that the application of PGPSD polysaccharide partially restored the pancreatic islets in diabetic mice, and enhanced the expression of pancreatic duodenal homeobox-1, insulin and hexokinase1. Collectively, the data suggested that the peach gum-derived polysaccharide had a meaningful potential as a non-insulin therapeutic compound in the treatment of diabetes.
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http://dx.doi.org/10.1016/j.ijbiomac.2017.01.085DOI Listing
May 2017

Gene Expression Changes during the Gummosis Development of Peach Shoots in Response to Lasiodiplodia theobromae Infection Using RNA-Seq.

Front Physiol 2016 9;7:170. Epub 2016 May 9.

Key Laboratory of Horticultural Plant Biology, Ministry of Education, Huazhong Agricultural University Wuhan, China.

Lasiodiplodia theobromae is a causal agent of peach (Prunus persica L.) tree gummosis, a serious disease affecting peach cultivation and production. However, the molecular mechanism underlying the pathogenesis remains unclear. RNA-Seq was performed to investigate gene expression in peach shoots inoculated or mock-inoculated with L. theobromae. A total of 20772 genes were detected in eight samples; 4231, 3750, 3453, and 3612 differentially expressed genes were identified at 12, 24, 48, and 60 h after inoculation, respectively. Furthermore, 920 differentially co-expressed genes (515 upregulated and 405 downregulated) were found, respectively. Gene ontology annotation revealed that phenylpropanoid biosynthesis and metabolism, uridine diphosphate-glucosyltransferase activity, and photosynthesis were the most differentially regulated processes during gummosis development. Significant differences were also found in the expression of genes involved in glycometabolism and in ethylene and jasmonic acid biosynthesis and signaling. These data illustrate the dynamic changes in gene expression in the inoculated peach shoots at the transcriptome level. Overall, gene expression in defense response and glycometabolism might result in the gummosis of peach trees induced by L. theobromae.
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http://dx.doi.org/10.3389/fphys.2016.00170DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4861008PMC
May 2016

Protection against MPP(+)-induced neurotoxicity in SH-SY5Y cells by tormentic acid via the activation of PI3-K/Akt/GSK3β pathway.

Neurochem Int 2016 07 16;97:117-23. Epub 2016 Mar 16.

Department of Applied Biology and Chemical Technology, The Hong Kong Polytechnic University, Hong Kong, China; Shenzhen Research Institute of the Hong Kong Polytechnic University, State Key Laboratory of Chinese Medicine and Molecular Pharmacology (Incubation), Shenzhen, Guangdong, China. Electronic address:

The cause of Parkinson's disease (PD) could be ascribed to the progressive and selective loss of dopaminergic neurons in the substantia nigra pars compacta, and thus molecules with neuroprotective ability may have therapeutic value against PD. In the current study, the neuroprotective effects and underlying mechanisms of tormentic acid (TA), a naturally occurring triterpene extracted from medicinal plants such as Rosa rugosa and Potentilla chinensis, were evaluated in a widely used cellular PD model in which neurotoxicity was induced by MPP(+) in cultured SH-SY5Y cells. We found that TA at 1-30 μM substantially protected against MPP(+)-induced neurotoxicity, as evidenced by the increase in cell viability, decrease in lactate dehydrogenase release and the reduction in apoptotic nuclei. Moreover, TA effectively inhibited the elevated intracellular accumulation of reactive oxygen species as well as Bax/Bcl-2 ratio caused by MPP(+). Most importantly, TA markedly reversed the inhibition of protein expression of phosphorylated Akt (Ser 473) and phosphorylated GSK3β (Ser 9) caused by MPP(+). LY294002, the specific inhibitor of PI3-K, significantly abrogated the up-regulated phosphorylated Akt and phosphorylated GSK3β offered by TA, suggesting that the neuroprotection of TA was mainly dependent on the activation of PI3-K/Akt/GSK3β signaling pathway. The results taken together indicate that TA may be a potential candidate for further preclinical study aimed at the prevention and treatment of PD.
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http://dx.doi.org/10.1016/j.neuint.2016.03.010DOI Listing
July 2016

The Dual Roles of Zinc Sulfate in Mitigating Peach Gummosis.

Plant Dis 2016 Feb 19;100(2):345-351. Epub 2015 Dec 19.

Key Laboratory of Horticultural Plant Biology, Huazhong Agricultural University, Ministry of Education, Wuhan, 430070, China.

Peach gummosis, caused by Lasiodiplodia theobromae, is one of the most prevalent diseases that affects peach production. In this study, we investigated the effect of zinc sulfate on inoculated peach shoots, as well as on the growth, morphology, and pathogenicity of L. theobromae in vitro, in the laboratory. Zinc deficiency was detected in diseased peach shoots by micronutrient analysis (Cu, Mn, and Zn) and confirmed by the measurement of transcript levels of zinc transporters (ZIP4, HAM4, and ZAT). The zinc was transferred from the diseased peach shoots to the peach gum. Applying zinc sulfate to the diseased peach shoots reduced the severity of peach gummosis, showing significantly reduced lesion size and gum weight, as well as downregulation of cell wall degradation-related gene (PG and PME) compared with the control. Zinc sulfate also specifically controlled peach gummosis under L. theobromae phytotoxin stress and induced the expression of defense-related genes (PR4, CHI, PAL, PGIP, and GNS3). In addition, in vitro mycelial growth of L. theobromae was significantly inhibited by zinc sulfate compared with the control. Zinc sulfate caused abnormal hyphae at 25 mM and swelling hyphal tips at 50 mM. Exposure of L. theobromae to zinc sulfate for 20 min inhibited the ability of the pathogen to cause peach gummosis. Our physiological and molecular data demonstrated that zinc sulfate has a dual function by reducing susceptibility in the host and by direct inhibition of the pathogen.
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http://dx.doi.org/10.1094/PDIS-01-15-0131-REDOI Listing
February 2016
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