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CsABF3-activated CsSUT1 pathway is implicated in pre-harvest water deficit inducing sucrose accumulation in citrus fruit

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Horticultural Plant Journal 2024年第1期10卷 103-114页

作者： Xiaochuan Ma Yuanyuan Chang Feifei Li Junfeng Yang Li Ye Tie Zhou Yan Jin Ling Sheng Xiaopeng Lu College of Horticulture Hunan Agricultural UniversityChangshaHunan 410128China National Center for citrus Improvement ChangshaHunan 410128China Institute of Horticulture Hunan Academy of Agricultural ScienceChangshaHunan 410125China

Pre-harvest water deficit(PHWD)plays an important role in sugar accumulation of citrus fruit.However,the mechanism is not known well.Here,it was confirmed that PHWD promoted sucrose accumulation of citrus fruit,but had limited effect on fructose,glucose and total acid.A sucrose transporter,Cs SUT1,which localizes to the plasma membrane,was demonstrated to function in sucrose transport induced by PHWD.Compared to wild-type,Cs SUT1 overexpression in citrus calli stimulated sucrose,fructose and glucose accumulation,while its silencing in juice sacs reduced sucrose accumulation.Increased sugar accumulation in transgenic lines enhanced plant drought tolerance,and resulted in decreased electrolyte leakage,malondialdehyde and hydrogen peroxide contents,as well as increased superoxide dismutase activity and proline contents.An abscisic acid(ABA)-responsive transcription factor,Cs ABF3,was found with a same expression pattern with Cs SUT1 under PHWD.Yeast one-hybrid,electrophoretic mobility shift assay and dual-luciferase assays all revealed that Cs ABF3 directly bound with the Cs SUT1 promoter by ABA responsive elements.When Cs ABF3 was overexpressed in citrus calli,the sucrose,fructose and glucose concentration increased correspondingly.Further,transgenic studies demonstrated that Cs ABF3 could affect sucrose accumulation by regulating Cs SUT1.Overall,this study revealed a regulation of Cs ABF3 promoting Cs SUT1 expression and sucrose accumulation in response to PHWD.Our results provide a detail insight into the quality formation of citrus fruit.

关键词： citrus Water deficit Pre-harvest Sucrose CsABF3 CsSUT1

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Improved observation of colonized roots reveals the regulation of arbuscule development and senescence by drought stress in the arbuscular mycorrhizae of citrus

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Horticultural Plant Journal 2024年第2期10卷 425-436页

作者： Xilong Yin Wei Zhang Zengwei Feng Guangda Feng Honghui Zhu Qing Yao College of Horticulture South China Agricultural UniversityKey Laboratory of Biology and Genetic Improvement of Horticultural Crops(South China)Ministry of Agriculture and Rural AffairsGuangdong Province Key Laboratory of Microbial Signals and Disease ControlGuangzhouGuangdong 510642China Key Laboratory of Agricultural Microbiomics and Precision Application Ministry of Agriculture and Rural AffairsGuangdong Provincial Key Laboratory of Microbial Culture Collection and ApplicationKey Laboratory of Agricultural MicrobiomicsState Key Laboratory of Applied Microbiology Southern ChinaGuangdong Microbial Culture Collection Center(GDMCC)Institute of MicrobiologyGuangdong Academy of SciencesGuangzhouGuangdong 510070China

citrus is the typical mycorrhizal fruit tree species establishing symbiosis with arbuscular mycorrhizal (AM) fungi. However, arbuscule development and senescence in colonized citrus roots, especially in response to drought stress, remain unclear, which is mainly due to the difficulty in clearing and staining lignified roots with the conventional method. Here, we improved the observation of colonized roots of citrus plants with the sectioning method, which enabled the clear observation of AM fungal structures. Furthermore, we investigated the effects of one week of drought stress on arbuscule development and senescence with the sectioning method. Microscopy observations indicated that drought stress significantly decreased mycorrhizal colonization (F%and M%) although it did not affect plant growth performance. Fluorescence probes (WGA 488 and/or Nile red) revealed that drought stress inhibited arbuscule development by increasing the percentage of arbuscules at the early stage and decreasing the percentages of arbuscules at the midterm and mature stages. Meanwhile, drought stress accelerated arbuscule senescence, which was characterized by the increased accumulation of neutral lipids. Overall, the sectioning method developed in this study enables the in-depth investigation of arbuscule status, and drought stress can inhibit arbuscule development but accelerate arbuscule senescence in the colonized roots of citrus plants. This study paves the way to elaborately dissecting the arbuscule dynamics in the roots of fruit tree species in response to diverse abiotic stresses.

关键词： Arbuscular mycorrhizae citrus Drought stress Arbuscule development Arbuscule senescence Fruit tree species

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Global analysis of basic leucine zipper transcription factors in trifoliate orange and the function identification of PtbZIP49 in salt tolerance

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Horticultural Plant Journal 2024年第1期10卷 115-130页

作者： Yuanyuan Xu Qiuling Hui Meng Li Hongxian Peng Yizhong He Changpin Chun Liangzhi Peng Xingzheng Fu National citrus Engineering Research Center Citrus Research InstituteSouthwest UniversityChongqing 400712China

As one of the most widely distributed and highly conserved transcription factors in eukaryotes,basic leucine zipper proteins(bZIPs)are involved in a variety of biological processes in plants,but they are largely unknown in citrus.In this study,56 bZIP family members were identified genome-wide from an important citrus rootstock,namely trifoliate orange(Poncirus trifoliata L.Raf.),and these putative bZIPs were named PtbZIP1—PtbZIP56.All PtbZIPs were classified into 13 subgroups by phylogenetic comparison with Arabidopsis thaliana bZIPs(AtbZIPs),and they were randomly distributed on nine known(50 genes)chromosomes and one unknown(6 genes)chromosome.Sequence analysis revealed the detailed characteristics of PtPZIPs,including their amino acid length,isoelectric point(pI),molecular weight(MW),predicted subcellular localization,gene structure,and conserved motifs.Prediction of promoter elements suggested the presence of drought,low-temperature,wound,and defense and stress responsive elements,as well as multiple hormone-responsive cis-acting elements.Spatiotemporal expression analysis showed the transcriptional patterns of PtbZIPs in different tissues and under dehydration,high salt,ABA,and IAA treatments.In addition,21 PtbZIPs were predicted to have direct or indirect protein—protein interactions.Among these,PtbZIP49 was experimentally proven to interact with PtbZIP1 or PtbZIP11 by using a yeast two-hybrid assay and bimolecular fluorescence complementation(BiFC).Subcellular localization analysis further revealed that PtbZIP1,PtbZIP11,and PtbZIP49 were localized in the nucleus.Moreover,PtbZIP49 was functionally identified as having an important role in salt stress via ectopic expression in A.thaliana and silenced in trifoliate orange using virus-induced gene silencing(VIGS).This study provided comprehensive information on PtbZIP transcription factors in citrus and highlights their potential functions in abiotic stress.

关键词： bZIP citrus Trifoliate orange Abiotic stress Expression pattern

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citrus Pan-Genome to Breeding Database(CPBD):A comprehensive genome database for citrus breeding

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Molecular Plant 2022年第10期15卷 1503-1505页

作者： Hanmingzi Liu Xia Wang Shengjun Liu Yue Huang Yi-Xiong Guo Wen-Zhao Xie Hao Liu Muhammad Tahir ul Qamar Qiang Xu Ling-Ling Chen College of Informatics Huazhong Agricultural UniversityWuhan 430070China Key Laboratory of Horticultural Plant Biology of Ministry of Education Huazhong Agricultural UniversityWuhan 430070China State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources College of Life Science and TechnologyGuangxi UniversityNanning 530004China Hubei Hongshan Laboratory Wuhan 430070China

Dear Editor,The genus citrus comprises more than 30 species worldwide(Swingle,1943).However,citrus genetics and traditional breeding are hindered due to asexual reproduction,long generation time,and empirical utilization of the germplasm.The whole-genome information of different citrus species accelerates the genetic studies and improves the breeding efficiency by high-density markers.

关键词： breeding citrus citrus

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A bZIP transcription factor(CiFD) regulates drought-and low-temperature-induced flowering by alternative splicing in citrus

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Journal of Integrative Plant Biology 2023年第3期65卷 674-691页

作者： Li-Xia Ye Yan-Mei Wu Jin-Xia Zhang Jin-Xin Zhang Huan Zhou Ren-Fang Zeng Wei Xuan Zheng Mei-Qi Qiu Jing-Jing Zhou Zong-Zhou Xie Chun-Gen Hu Jin-Zhi Zhang Key Laboratory of Horticultural Plant Biology(Ministry of Education) College of Horticulture and Forestry ScienceHuazhong Agricultural UniversityWuhan 430070China Institute of Fruit and Tea Hubei Academy of Agricultural SciencesWuhan 430064China

Drought and low temperature are two key environmental factors that induce adult citrus flowering. However, the underlying regulation mechanism is poorly understood. The bZIP transcription factor FD is a key component of the florigen activation complex(FAC) which is composed of FLOWERING LOCUS T(FT), FD, and 14-3-3 proteins. In this study, isolation and characterization of CiFD in citrus found that there was alternative splicing(AS) of CiFD, forming two different proteins(CiFDα and CiFDβ). Further investigation found that their expression patterns were similar in different tissues of citrus, but the subcellular localization and transcriptional activity were different. Overexpression of the CiFD DNA sequence(CiFD-DNA), CiFDα, or CiFDβ in tobacco and citrus showed early flowering, and CiFD-DNA transgenic plants were the earliest, followed by CiFDβ and CiFDα. Interestingly, CiFDα and CiFDβ were induced by low temperature and drought, respectively. Further analysis showed that CiFDαcan form a FAC complex with CiFT, Ci14-3-3, and then bind to the citrus APETALA1(CiAP1) promoter and promote its expression. However,CiFDβ can directly bind to the CiAP1 promoter independently of CiFT and Ci14-3-3. These results showed that CiFDβ can form a more direct and simplified pathway that is independent of the FAC complex to regulate drought-induced flowering through AS. In addition, a b HLH transcription factor(CibHLH96) binds to CiFD promoter and promotes the expression of CiFD under drought condition. Transgenic analysis found that CibHLH96 can promote flowering in transgenic tobacco. These results suggest that CiFD is involved in drought-and low-temperature-induced citrus flowering through different regulatory patterns.

关键词： alternative splicing citrus CiFD drought flowering low temperature

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Transcription factor CsESE3 positively modulates both jasmonic acid and wax biosynthesis in citrus

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aBIOTECH 2022年第4期3卷 250-266页

作者： Haoliang Wan Haiji Qiu Zhuoran Li Xiaoliang Zhang Jingyu Zhang Deyuan Jiang Alisdair RFernie Yi Lyu Yunjiang Cheng Weiwei Wen Key Laboratory of Horticultural Plant Biology(MOE) College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhan430070China Shenzhen Institute of Nutrition and Health Huazhong Agricultural UniversityWuhan430070China Shenzhen Branch Guangdong Laboratory for Lingnan Modern AgricultureGenome Analysis Laboratory of the Ministry of AgricultureAgricultural Genomics Institute at ShenzhenChinese Academy of Agricultural SciencesShenzhen518000China Max-Planck-Institute of Molecular Plant Physiology Am Muehlenberg 114476PotsdamGermany Key Laboratory for Space Bioscience and Biotechnology School of Life SciencesNorthwestern Polytechnical UniversityXi’an710072China

PLIP lipases can initiate jasmonic acid(JA)biosynthesis.However,little is known about the transcriptional regulation of this process.In this study,an ERF transcription factor(CsESE3)was found to be co-expressed with all necessary genes for JA biosynthesis and several key genes for wax biosynthesis in transcriptomes of‘Newhall’navel orange.CsESE3 shows partial sequence similarity to the well-known wax regulator SHINEs(SHNs),but lacks a complete MM protein domain.Ectopic overexpression of CsESE3 in tomato(OE)resulted in reduction of fruit surface brightness and dwarf phenotype compared to the wild type.The OE tomato lines also showed significant increases in the content of wax and JA and the expression of key genes related to their biosynthesis.Overexpression of CsESE3 in citrus callus and fruit enhanced the JA content and the expression of JA biosynthetic genes.Furthermore,CsESE3 could bind to and activate the promoters of two phospholipases from the PLIP gene family to initiate JA biosynthesis.Overall,this study indicated that CsESE3 could mediate JA biosynthesis by activating PLIP genes and positively modulate wax biosynthesis.The findings provide important insights into the coordinated control of two defense strategies of plants represented by wax and JA biosynthesis.

关键词： citrus Cuticular wax Jasmonic acid SHINE transcription factor Lipase

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An efficient transient gene expression system for protein subcellular localization assay and genome editing in citrus protoplasts

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Horticultural Plant Journal 2023年第3期9卷 425-436页

作者： Wenhui Yang Jiaqin Ren Wanrong Liu Dan Liu Kaidong Xie Fei Zhang Pengwei Wang Wenwu Guo Xiaomeng Wu National Key Laboratory for Germplasm Innovation&Utilization of Horticultural Crops College of Horticulture and Forestry SciencesHuazhong Agricultural UniversityWuhanHubei 430070China Hubei Hongshan Laboratory WuhanHubei 430070China

Protoplast has been widely used in biotechnologies to circumvent the breeding obstacles in citrus, including long juvenility, polyembryony, and male/female sterility. The protoplast-based transient gene expression system is a powerful tool for gene functional characterization and CRISPR/Cas9 genome editing in higher plants, but it has not been widely used in citrus. In this study, the polyethylene glycol(PEG)-mediated method was optimized for citrus callus protoplast transfection, with an improved transfection efficiency of 68.4%. Consequently, the efficiency of protein subcellular localization assay was increased to 65.8%, through transient expression of the target gene in protoplasts that stably express the fluorescent organelle marker protein. The gene editing frequencies in citrus callus protoplasts reached 14.2% after transient expression of CRISPR/Cas9 constructs. We demonstrated that the intronic polycistronic tRNAgRNA(inPTG) genome editing construct was functional in both the protoplast transient expression system and epicotyl stable transformation system in citrus. With this optimized protoplast transient expression system, we improved the efficiency of protein subcellular localization assay and developed the genome editing system in callus protoplasts, which provides an approach for prompt test of CRISPR vectors.

关键词： citrus Callus protoplast Transient transfection Subcellular localization Genome editing

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The constitutions of terpenoids and hormones of leaves in red-flesh citrus mutants and their wild types

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Horticultural Plant Journal 2022年第3期8卷 297-310页

作者： Cuihua Liu Min He Juan Xu College of Horticulture Northwest A&F UniversityYangling 712100ShaanxiChina Key Laboratory of Horticultural Plant Biology(Ministry of Education) College of Horticulture and ForestryHuazhong Agricultural UniversityWuhan 430070China

To study the profiles and relationships of terpenoids and phytohormones in leaves of red-flesh citrus,we examined four red-flesh mutants that accumulate lycopene in the fruit and their corresponding wild types.We compared their contents of monoterpenoid and sesquiterpenoid volatiles,triterpenoid limonoid aglycones,and tetraterpenoid carotenoids.The types and concentrations of these terpenoids in the leaves varied among genotypes,and the leaf terpenoid profiles differed between red-fleshmutants and theirwild types.However,lycopenewas not detected in citrus leaves of all eight varieties,including the fourmutants.According to phytohormone accumulation in the leaves,the citrus varieties could be classified into a low-phytohormone group(‘Red Anliu’sweet orange,‘Anliu’sweet orange,and‘Cara Cara’navel orange),a high-phytohormone group(‘Seike’navel orange),and a high-jasmonic acid group(‘Red-flesh Guanxi’pummelo,‘Guanxi’pummelo,‘Chuhong’pummelo,and‘Feicui’pummelo).The contents of terpenoid volatiles were very low in leaves of‘Red-flesh Guanxi’and‘Guanxi’pummelo;therefore,they are ideal materials for verifying the functions of genes related to terpenoid volatiles in overexpression analyses.Sesquiterpenoid volatiles were positively correlated with phytohormones of abscisic acid,jasmonic acid,and salicylic acid.Taken together,lycopene was undetected in the leaves of redflesh citrus mutants with abundant lycopene in their juice sacs,which suggested a tissue-specific accumulation pattern of lycopene in citrus red-flesh mutants.Furthermore,leaf volatile profiles could be suitable to develop fingerprint chromatograms of citrus resources,since leaf volatile profiles were dominated by several compounds that varied among genotypes in their combinations and concentrations.

关键词： citrus Carotenoid Terpenoid volatile Limonoid aglycone Hormone Leaf

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Mapping of QTLs and candidate genes associated with multiple phenotypic traits for Huanglongbing tolerance in citrus

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Horticultural Plant Journal 2023年第4期9卷 705-719页

作者： Ming Huang Mikeal L. Roose Qibin Yu Ed Stover David G. Hall Zhanao Deng Frederick G.Gmitter Jr. Key Laboratory of Plant Hormones and Development Regulation of Chongqing College of Life SciencesChongqing UniversityChongqing 401331China citrus Research and Education Center University of FloridaLake AlfredFL 33850United States Department of Botany and Plant Sciences University of CaliforniaRiversideCA 92521United States United States Horticultural Research Laboratory Agricultural Research ServiceUnited States Department of AgricultureFort PierceFL 34945United States Gulf Coast Research and Education Center University of FloridaWimaumaFL 33598United States

Huanglongbing(HLB)is the most devastating disease for citrus worldwide.Candidatus Liberibacter asiaticus(C Las),vectored by Asian citrus psyllid(ACP,Diaphorina citri Kuwayama),is the most common pathogen causing the disease.Commercial citrus varieties are highly susceptible to HLB,whereas trifoliate orange(Poncirus trifoliata)is considered highly tolerant to HLB.An F1 segregating population and their parent trifoliate orange and sweet orange,which had been exposed to intense HLB pressure for three years,was evaluated for disease symptoms,ACP colonization,C Las titer and tree vigor repeatedly for two to three years.Trifoliate orange and sweet orange showed significant differences for most of the phenotypic traits,and the F1 population exhibited a large variation.A high-density SNP-based genetic map with 1402 markers was constructed for trifoliate orange,which exhibited high synteny and high coverage of its reference genome.A total of 26 quantitative trait locus(QTLs)were identified in four linkage groups LG-t6,LG-t7,LG-t8 and LG-t9,of which four QTL clusters exhibit a clear co-localization of QTLs associated with different traits.Through genome-wide analysis of gene expression in response to C Las infection in‘Flying Dragon’and‘Larger-Flower DPI-50-7’trifoliate orange,85 differentially expressed genes were found located within the QTL clusters.Among them,seven genes were classified as defense or immunity protein which exhibited the highest transcriptional change after C Las infection.Our results indicate a quantitative genetic nature of HLB tolerance and identified candidate genes that should be valuable for searching for genetic solutions to HLB through breeding or genetic engineering.

关键词： Candidatus liberibacter QTL mapping Phenotyping F1 population Poncirus citrus

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Transcriptomic analysis reveals the defense mechanisms of citrus infested with Diaphorina citri

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Horticultural Plant Journal 2023年第3期9卷 450-462页

作者： Xueli Sun Ting Yu Minliang Bin Chunhua Hu Fangcheng Bi Xinxiang Peng Ganjun Yi Xinxin Zhang State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources College of Life SciencesSouth China Agricultural UniversityGuangzhouGuangdong 510642China Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization(MOA) Guangdong Province Key Laboratory of Tropical and Subtropical Fruit Tree ResearchInstitute of Fruit Tree ResearchGuangdong Academy of Agricultural SciencesGuangzhouGuangdong 510640China Agricultural Biological Gene Research Center Guangdong Academy of Agricultural SciencesGuangzhouGuangdong 510640China

Huanglongbing(HLB) is a devastating disease that has led to an acute crisis for growers of citrus, one of the world's most important fruit crops. The phloem-feeding Asian citrus psyllid(ACP), Diaphorina citri, is the main pest at the new shoot stage and is the only natural vector of HLB pathogenic bacteria. Little is known about how plants perceive and defend themselves from this destructive pest. Here, we characterized changes in the expression of various genes in citrus plants that were continuously infested by D. citri for different durations(12, 24, and 48 h). A total of 5 219 differentially expressed genes(DEGs) and 643 common DEGs were identified across all time points. Several pathways related to defense were activated, such as peroxisome, alpha-linolenic acid metabolism, and phenylpropanoid and terpenoid biosynthesis, and some pathways related to growth and signal transduction were suppressed in response to D. citri infestation. The expression of genes including kinases(CML44, CIPK6, and XTH6), phytohormones(SAMT, LOX6, and NPR3), transcription factors(bHLH162, WRKY70, and WRKY40), and secondary metabolite synthesis-related genes(PAL, 4CL2, UGT74B1 and CYP82G1) was significantly altered in response to D. citri infestation. The findings of this study greatly enhance our understanding of the mechanisms underlying the defense response of citrus plants to D. citri infestation at the molecular level. Functional characterization of the candidate defense-related genes identified in this study will aid the molecular breeding of insect-resistant citrus varieties.

关键词： Asian citrus psyllid citrus Diaphorina citri Huanglongbing Infestation RNA-seq

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