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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

The evolution and functional divergence of 10 Apolipoprotein D-like genes in Nilaparvata lugens

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Insect Science 2024年第1期31卷 91-105页

作者： Jia-Bao Lu Peng-Peng Ren Qiao Li Fang He Zhong-Tian Xu Sai-Nan Wang Jian-Ping Chen Jun-Min Li Chuan-Xi Zhang citrus Research Institute Southwest University/Chinese Academy of Agricultural SciencesNational Engineering Research Center for CitrusChongqingChina Technology center of Wuhan Customs District HubeiChina Institute of Insect Science Zhejiang UniversityHangzhouChina

Apolipoprotein D(ApoD),a member of the lipocalin superfamily of proteins,is involved in lipid transport and stress resistance.Whereas only a single copy of the ApoD gene is found in humans and some other vertebrates,there are typically several ApoD-like genes in insects.To date,there have been relatively few studies that have examined the evolution and functional differentiation of ApoD-like genes in insects,particularly hemi-metabolous insects.In this study,we identified 10 ApoD-like genes(NlApoD1−10)with distinct spatiotemporal expression patterns in Nilaparvata lugens(BPH),which is an important pest of rice.NlApoD1−10 were found to be distributed on 3 chromosomes in a tandem array of NlApoD1/2,NlApoD3−5,and NlApoD7/8,and show sequence and gene structural divergence in the coding regions,indicating that multiple gene duplication events occurred during evolution.Phylogenetic analysis revealed that NlApoD1−10 can be clustered into 5 clades,with NlApoD3−5 and NlApoD7/8 potentially evolving exclusively in the Delphacidae family.Functional screening using an RNA interference approach revealed that only NlApoD2 was essential for BPH development and survival,whereas NlApoD4/5 are highly expressed in testes,and might play roles in reproduction.Moreover,stress response analysis revealed that NlApoD3−5/9,NlApoD3−5,and NlApoD9 were up-regulated after treatment with lipopolysaccharide,H2O2,and ultraviolet-C,respectively,indicating their potential roles in stress resistance.

关键词： Apolipoprotein D BPH evolution functional divergence gene duplication NIApoD

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

Eureka lemon zinc finger protein ClDOF3.4 interacts with citrus yellow vein clearing virus coat protein to inhibit viral infection

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Journal of Integrative Agriculture 2024年第6期23卷 1979-1993页

作者： Ping Liao Ting Zeng Mengyang Huangfu Cairong Zheng Jiequn Ren Changyong Zhou Yan Zhou Integrative Science center of Germplasm Creation in Western China(CHONGQING)Science City Citrus Research InstituteSouthwest UniversityChongqing 400712China national citrus Engineering Research center Citrus Research InstituteSouthwest UniversityChongqing 400712China Chongqing Three Gorges Academy of Agricultural Science Chongqing Three Gorges UniversityChongqing 404020China

citrus yellow vein clearing virus(CYVCV)is a new citrus virus that has become an important factor restricting the development of China’s citrus industry,and the CYVCV coat protein(CP)is associated with viral pathogenicity.In this study,the Eureka lemon zinc finger protein(ZFP)ClDOF3.4 was shown to interact with CYVCV CP in vivo and in vitro.Transient expression of ClDOF3.4 in Eureka lemon induced the expression of salicylic acid(SA)-related and hypersensitive response marker genes,and triggered a reactive oxygen species burst,ion leakage necrosis,and the accumulation of free SA.Furthermore,the CYVCV titer in ClDOF3.4 transgenic Eureka lemon plants was approximately 69.4%that in control plants 6 mon after inoculation,with only mild leaf chlorotic spots observed in those transgenic plants.Taken together,the results indicate that ClDOF3.4 not only interacts with CP but also induces an immune response in Eureka lemon by inducing the SA pathways.This is the first report that ZFP is involved in the immune response of a citrus viral disease,which provides a basis for further study of the molecular mechanism of CYVCV infection.

关键词： citrus yellow vein clearing virus coat protein ClDOF3.4 plant immune response

High-throughput screening system of citrus bacterial cankerassociated transcription factors and its application to the regulation of citrus canker resistance

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Journal of Integrative Agriculture 2024年第1期23卷 155-165页

作者： Jia Fu Jie Fan Chenxi Zhang Yongyao Fu Baohang Xian Qiyuan Yu Xin Huang Wen Yang Shanchun Chen Yongrui He Qiang Li Integrative Science center of Germplasm Creation in Western China(Chongqing)Science City Citrus Research InstituteSouthwest UniversityChongqing 400712China School of Advanced Agriculture and Bioengineering Yangtze Normal UniversityChongqing 408100China national citrus Engineering Research center Chongqing 400712China

One of the main diseases that adversely impacts the global citrus industry is citrus bacterial canker(CBC),caused by the bacteria Xanthomonas citri subsp.citri(Xcc).Response to CBC is a complex process,with both proteinDNA as well as protein–protein interactions for the regulatory network.To detect such interactions in CBC resistant regulation,a citrus high-throughput screening system with 203 CBC-inducible transcription factors(TFs),were developed.Screening the upstream regulators of target by yeast-one hybrid(Y1H)methods was also performed.A regulatory module of CBC resistance was identified based on this system.One TF(CsDOF5.8)was explored due to its interactions with the 1-kb promoter fragment of CsPrx25,a resistant gene of CBC involved in reactive oxygen species(ROS)homeostasis regulation.Electrophoretic mobility shift assay(EMSA),dual-LUC assays,as well as transient overexpression of CsDOF5.8,further validated the interactions and transcriptional regulation.The CsDOF5.8–CsPrx25 promoter interaction revealed a complex pathway that governs the regulation of CBC resistance via H2O2homeostasis.The high-throughput Y1H/Y2H screening system could be an efficient tool for studying regulatory pathways or network of CBC resistance regulation.In addition,it could highlight the potential of these candidate genes as targets for efforts to breed CBC-resistant citrus varieties.

关键词： citrus bacterial canker(CBC) high-throughput screening system transcription factor(TF) yeast-one hybrid(Y1H) CsPrx25

Orchestrating seed storage protein and starch accumulation toward overcoming yield–quality trade-off in cereal crops

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Journal of Integrative Plant Biology 2024年第3期66卷 468-483页

作者： Shuanghe Cao Bingyan Liu Daowen Wang Awais Rasheed Lina Xie Xianchun Xia Zhonghu He State Key Laboratory of Crop Gene Resources and Breeding/national Wheat improvement center Institute of Crop SciencesBeijing 100081China College of Agronomy Henan Agricultural UniversityZhengzhou 450002China International Maize and Wheat improvement center(CIMMYT)China Office Chinese Academy of Agricultural SciencesBeijing 100081China

Achieving high yield and good quality in crops is essential for human food security and health.However,there is usually disharmony between yield and quality.Seed storage protein(SSP)and starch,the predominant components in cereal grains,determine yield and quality,and their coupled synthesis causes a yield–quality trade-off.Therefore,dissection of the underlying regulatory mechanism facilitates simultaneous improvement of yield and quality.Here,we summarize current findings about the synergistic molecular machinery underpinning SSP and starch synthesis in the leading staple cereal crops,including maize,rice and wheat.We further evaluate the functional conservation and differentiation of key regulators and specify feasible research approaches to identify additional regulators and expand insights.We also present major strategies to leverage resultant information for simultaneous improvement of yield and quality by molecular breeding.Finally,future perspectives on major challenges are proposed.

关键词： cereal crops grain yield and quality seed storage protein starch synergistic regulation

Haploids can be induced in knockout mutants of OsPLA1,but not OsDMP3 or OsDMP6,in rice

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The Crop Journal 2024年第1期12卷 213-221页

作者： Zongkai Liu Yu Zhong Xiaolong Qi Tai An Shuwei Guo Dong Wang Yuwen Wang Bin Feng Zuofeng Zhu Shaojiang Chen Chenxu Liu national Maize improvement center Engineering Research Center of Ministry of EducationChina Agricultural UniversityBeijing 100193China national center for Evaluation of Agricultural Wild Plants(Rice) Department of Plant Genetics and BreedingChina Agricultural UniversityBeijing 100193China

Doubled haploid(DH)technology is an important tool in crop breeding because it can significantly accelerate the breeding process.ZmPLA1/MATL/NLD and ZmDMP are two key genes controlling haploid induction(HI)in maize,exhibiting a synergistic effect.However,it is unknown whether knock out of ZmDMP orthologs can stimulate HI in rice.In this study,a ZmPLA1 ortholog(OsPLA1)and two ZmDMP orthologs(OsDMP3 and OsDMP6)were identified in rice.All three genes encode plasma membrane-localized proteins and were highly expressed in mature anthers.Knockout of OsPLA1 in both Minghui 63 and Nipponbare resulted in reduced seed setting rate(SSR)and caused HI.The osdmp3,osdmp6 and the double mutant failed to trigger HI independently,nor increased the haploid induction rate(HIR)when combined with ospla1.Repeated pollinations operations of QX654A with the ospla1 mutant significantly improve SSR,while reducing HIR.RNA-seq profiling of mature ospla1 mutant anthers indicated that a large number of differentially expressed genes(DEGs)were enriched in redox homeostasis and lipid metabolic GO terms,plant hormone signal transduction,and MAPK signaling pathways.These findings provide important insights towards construction of an efficient DH breeding technology and study of the molecular mechanism of HI in rice.

关键词： Doubled haploid breeding Haploid induction Mutation anlaysis Rice

Oriented Generation of Novel Thermo-Sensitive Genic Male Sterile Lines with Improved Grain Shape and Outcrossing Rate in Early-Season Rice

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Rice science 2024年第2期31卷 129-133,I0001-I0016页

作者： ZHANG Huali CHEN Junyu LI Ruiqing WANG Huimei DAI Dongqing LIANG Minmin WU Mingyue MA Liangyong State Key Laboratory of Rice Biology and Breeding/Chinese national center for Rice improvement China National Rice Research InstituteHangzhou 310006China

Two-line hybrid rice with excellent quality is preferred in the Chinese market.However,there is a trade-off between reducing costs for hybrid seed production and lowering the outcrossing rate of the sterile line,which is largely determined by the stigma exsertion rate(SER).In this study,we constructed mutants of male sterility lines with improved grain length(GL)and SER in three elite early-season indica rice varieties through targeted manipulation of the TMS5 and GS3 genes using CRISPR/Cas9-mediated multiplex systems.We obtained a series of marker-free gs3 single mutants and gs3tms5 double mutants with significantly higher SER,longer grains,and increased 1000-grain weight compared with the wild type(WT).Importantly,the typically thermo-sensitive genic male sterile(TGMS)trait with a higher SER was observed in gs3tms5 mutants,and their F1 hybrids exhibited remarkable improvements in grain shape and yield-related traits.Our findings provided an efficient method to generate new valuable TGMS germplasm with improved SER through the mutagenesis of GS3 and TMS5 synergistically,and demonstrated that GS3 had pleiotropic effects on grain size,SER,and grain quality in early-season indica rice.

关键词： sterile elite season

OsbZIP01 Affects Plant Growth and Development by Regulating OsSD1 in Rice

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Rice science 2024年第1期31卷 77-86,I0018,I0019页

作者： DONG Xinli ZHOU Yang ZHANG Yaqi RONG Fuxi DU Jiahong HONG Zheyuan HU Peisong LÜYusong College of Agriculture and Biotechnology Zhejiang UniversityHangzhou 310058China State Key Laboratory of Rice Biology and Breeding/China national center for Rice improvement China National Rice Research InstituteHangzhou 310006China

As the‘Green Revolution’gene,SD1(encoding GA20ox2),has been widely applied to improve yield in rice breeding.However,research on its transcriptional regulation is limited.Here,we identified a transcription factor OsbZIP01,which can suppress the expression of SD1 and regulate gibberellin(GA)biosynthesis in rice.Knockout mutants of OsbZIP01 exhibited increased plant height,while the overexpression lines showed a semi-dwarf phenotype and diminished germination rate.Furthermore,the semi-dwarf phenotype of OE-bZIP01,was caused by the reduced internode length,which was accompanied by a thin stem width.The predominant expression of OsbZIP01 was observed in leaves and sheaths.OsbZIP01 protein was localized in the nucleus and showed transcriptional repression activity.In addition,OsbZIP01 could directly bind to the promoter of the OsSD1 gene,and inhibit its transcription.The semi-dwarf phenotype of OE-bZIP01 could be rescued by exogenous GA_(3).Meanwhile,the bzip01 sd1 double mutant showed a shorter shoot length compared with the wild type,indicating that OsbZIP01 regulated plant growth mainly through the GA biosynthesis pathway.Collectively,OsbZIP01 negatively regulates GA biosynthesis by restraining SD1 transcription,thereby affecting plant growth and development.

关键词： OsbZIP01 SD1 gibberellin biosynthesis dwarf and germination