Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (8): 2525-2540    DOI: 10.1016/j.jia.2023.12.004
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Exploring the genetic basis of pre-harvest sprouting in rice through a genome-wide association study-based haplotype analysis
Myeong-Hyeon Min1, Aye Aye Khaing2, Sang-Ho Chu1, Bhagwat Nawade1, Yong-Jin Park1

1 Department of Plant Resources, College of Industrial Sciences, Kongju National University, Yesan 32439, Republic of Korea

2 Department of Agronomy, Yezin Agricultural University, Nay Pyi Taw 15013, Myanmar

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  

In this study, we employed genome-wide association studies (GWAS) on diverse rice accessions to identify novel PHS-associated haplotypes.  An assessment of 127 cultivated accessions for panicle germination (PHS) and detached grain germination (germination rate of detached grains at the 14th day (D14)) revealed considerable phenotypic variation among rice ecotypes.  GWAS analysis identified 91 significant signals at –log10(P-value)>5, including 15 SNPs for PHS and 76 SNPs for D14.  A subsequent linkage disequilibrium (LD) block-based GWAS analysis detected 227 significant SNPs for both traits, consisting of 18 nonsynonymous substitutions located on the coding regions of nine genes.  Further haplotype analysis identified 32 haplotypes, with 10 specific to cultivated accessions, 19 specific to the wild type, and three shared between them.  A phenotypic assessment of major haplotypes revealed significant differences between resistant (Hap1 and Hap2) and susceptible haplotypes (Hap5, Hap27, and Hap28), distinguished by a G/A SNP within a novel gene, Os04g0545200.  The identified haplotypes offer promising prospects for haplotype-based breeding aimed at enhancing PHS resistance in rice.

Keywords:  rice       PHS        dormancy        germination        GWAS        haplotype        abiotic stress  
Received: 07 August 2023   Accepted: 24 October 2023
Fund: 
This work was supported by the National Research Foundation of Korea (NRF) grants funded by the Ministry of Science and Information and Communication Technology (MSIT), Republic of Korea (NRF-2022R1A4A1030348 and 2023R1A2C1004432) and the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture and Forestry (IPET) through the Digital Breeding Transformation Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA), Republic of Korea (322060031HD020), and the Cooperative Research Program for Agriculture Science and Technology Development, Rural Development Administration, Republic of Korea (RS-2023-00222739).
About author:  #Correspondence Yong-Jin Park, Tel: +82-41-330-1201, Fax: +82-41-330-1209, E-mail: yjpark@kongju.ac.kr

Cite this article: 

Myeong-Hyeon Min, Aye Aye Khaing, Sang-Ho Chu, Bhagwat Nawade, Yong-Jin Park. 2024. Exploring the genetic basis of pre-harvest sprouting in rice through a genome-wide association study-based haplotype analysis. Journal of Integrative Agriculture, 23(8): 2525-2540.

Ali F, Qanmber G, Li F, Wang Z. 2022. Updated role of ABA in seed maturation, dormancy, and germination. Journal of Advanced Research, 35, 199–214.

Barrett J C, Fry B, Maller J, Daly M J. 2005. Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics21, 263–265.

Bevan M W, Uauy C, Wulff B B H, Zhou J, Krasileva K, Clark M D. 2017. Genomic innovation for crop improvement. Nature, 543, 346–354.

Bradbury P J, Zhang Z, Kroon D E, Casstevens T M, Ramdoss Y, Buckler E S. 2007. TASSEL: Software for association mapping of complex traits in diverse samples. Bioinformatics, 23, 2633–2635.

Chen W, Wang W, Lyu Y, Wu Y, Huang P, Hu S, Wei X, Jiao G, Sheng Z, Tang S, Shao G, Luo J. 2021. OsVP1 activates Sdr4 expression to control rice seed dormancy via the ABA signaling pathway. The Crop Journal, 9, 68–78.

Danecek P, Auton A, Abecasis G, Albers C A, Banks E,  DePristo A M, Handsaker E R, Lunter G, Marth T G, Sherry T S, McVean G, Durbin R, 1000 Genomes Project Analysis Group. 2011. The variant call format and VCFtools. Bioinformatics27, 2156–2158.

Day P M. 2008. Phosphatidylinositol 3-kinase is a positive regulator of gibberellin signaling. Ph thesis, The Pennsylvania State University, USA.

Deng X, An B, Zhong H, Yang J, Kong W, Li Y. 2019. A Novel insight into functional divergence of the MST gene family in rice based on comprehensive expression patterns. Genes10, 239.

Fernie A R, Gutierrez-Marcos J. 2019. From genome to phenome: Genome-wide association studies and other approaches that bridge the genotype to phenotype gap. The Plant Journal97, 5–7.

Finch-Savage W E, Leubner-Metzger G. 2006. Seed dormancy and the control of germination. New Phytologist171, 501–523.

Finkelstein R, Reeves W, Ariizumi T, Steber C. 2008. Molecular aspects of seed dormancy. Annual Review of Plant Biology59, 387–415.

Francis R M. 2017. Pophelper: An R package and web app to analyse and visualize population structure. Molecular Ecology Resources, 17, 27–32.

Fu K, Song W, Chen C, Mou C, Huang Y, Zhang F, Hao Q, Wang P, Ma T, Chen Y, Zhu Z. 2022. Improving pre-harvest sprouting resistance in rice by editing OsABA8ox using CRISPR/Cas9. Plant Cell Reports, 41, 2107–2110.

Gabriel S B, Schaffner S F, Nguyen H, Moore J M, Roy J, Blumenstiel B, Higgins J, DeFelice M, Lochner A, Faggart M, Liu-Cordero S N. 2002. The structure of haplotype blocks in the human genome. Science296, 2225–2229.

Ge S X, Jung D, Yao R. 2020. ShinyGO: A graphical gene-set enrichment tool for animals and plants. Bioinformatics, 36, 2628–2629.

Gu X Y, Chen Z X, Foley M E. 2003. Inheritance of seed dormancy in weedy rice. Crop Science, 43, 835–843.

Haake V, Cook D, Riechmann J L, Pineda O, Thomashow M F, Zhang J Z. 2002. Transcription factor CBF4 is a regulator of drought adaptation in ArabidopsisPlant Physiology130, 639–648.

Hou M Y, Wang C M, Jiang L, Wan J M, Yasui H, Yoshimura A. 2004. Inheritance and QTL mapping of low temperature germinability in rice (Oryza sativa L.). Acta Genetica Sinica31, 701–706. (in Chinese)

Hu Y, Zhao L, Chong K, Wang T. 2008. Overexpression of OsERF1, a novel rice ERF gene, up-regulates ethylene-responsive genes expression besides affects growth and development in ArabidopsisJournal of Plant Physiology, 165, 1717–1725.

Huang X, Kurata N, Wei X, Wang Z X, Wang A, Zhao Q, Zhao Y, Liu K, Lu H, Li W, Guo Y, Lu Y, Zhou C, Fan D, Weng Q, Zhu C, Huang T, Zhang L, Wang Y, Feng L, et al. 2012. A map of rice genome variation reveals the origin of cultivated rice. Nature490, 497–501.

Jain M, Khurana J P. 2009. Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. The FEBS Journal, 276, 3148–3162.

Jang S G, Kim B, Choi I, Lee J, Ham T H, Kwon S W. 2023. Fine-mapping analysis of the genes associated with pre-harvest sprouting tolerance in rice (Oryza sativa L.). Agronomy13, 818.

Kermode A R, Bewley J D. 1989. Developing seeds of Ricinus communis L., when detached and maintained in an atmosphere of high relative humidity, switch to a germinative mode without the requirement for complete desiccation. Plant Physiology90, 702–707.

Kim K W, Chung H K, Cho G T, Ma K H, Chandrabalan D, Gwag J G, Kim T S, Cho E G, Park Y J. 2007. PowerCore: A program applying the advanced M strategy with a heuristic search for establishing core sets. Bioinformatics23, 2155–2162.

Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

Lan J, Lin Q, Zhou C, Ren Y, Liu X, Miao R, Jing R, Mou C, Nguyen T, Zhu X, Wang Q, Zhang X, Guo X, Liu S, Jiang L, Wan J. 2020. Small grain and semi-dwarf 3, a WRKY transcription factor, negatively regulates plant height and grain size by stabilizing SLR1 expression in rice. Plant Molecular Biology, 104429–450.

Lee G A, Jeon Y A, Lee H S, Hyun D Y, Lee J R, Lee M C, Lee S Y, Ma K H, Koh H J. 2017. New genetic loci associated with preharvest sprouting and its evaluation based on the model equation in rice. Frontiers in Plant Science, 81393.

Lee G A, Jeon Y A, Lee H S, Hyun D Y, Lee J R, Lee M C, Lee S Y, Ma K H, Koh H J. 2018. Variation in pre-harvest sprouting resistance, seed germination and changes in abscisic acid levels during grain development in diverse rice genetic resources. Plant Genetic Resources, 16, 18–27.

Lee J, Kwon S W. 2015. Analysis of quantitative trait loci associated with seed germination and coleoptile length under low temperature condition. Journal of Crop Science and Biotechnology18, 273–278.

Lee J S, Chebotarov D, McNally K L, Pede V, Setiyono T D, Raquid R, Hyun W J, Jeung J U, Kohli A, Mo Y. 2021. Novel sources of pre-harvest sprouting resistance for japonica rice improvement. Plants10, 1709.

Leubner-Metzger G, Petruzzelli L, Waldvogel R, Vögeli-Lange R, Meins F. 1998. Ethylene-responsive element binding protein (EREBP) expression and the transcriptional regulation of class I β-1,3-glucanase during tobacco seed germination. Plant Molecular Biology38, 785–795.

Liang S, Xiong W, Yin C, Xie X, Jin Y J, Zhang S, Yang B, Ye G, Chen S, Luan W J. 2019. Overexpression of OsARD1 improves submergence, drought, and salt tolerances of seedling through the enhancement of ethylene synthesis in rice. Frontiers in Plant Science, 10, 1088.

Licausi F, Ohme-Takagi M, Perata P. 2013. APETALA2/ethylene responsive factor (AP2/ERF) transcription factors: Mediators of stress responses and developmental programs. The New Phytologist, 199, 639–649.

Lipka A E, Tian F, Wang Q, Peiffer J, Li M, Bradbury P J, Gore M A, Buckler E S, Zhang Z. 2012. GAPIT: Genome association and prediction integrated tool. Bioinformatics28, 2397–2399.

Liu L, Xia W, Li H, Zeng H, Wei B, Han S, Yin C. 2018. Salinity inhibits rice seed germination by reducing α-amylase activity via decreased bioactive gibberellin content. Frontiers in Plant Science9275.

Liu J, Zhou J, Xing D. 2012. Phosphatidylinositol 3-kinase plays a vital role in regulation of rice seed vigor via altering NADPH oxidase activity. PLoS ONE7, e33817.

Lo S F, Yang S Y, Chen K T, Hsing Y I, Zeevaart J A D, Chen L J, Yu S M. 2008. A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. The Plant Cell, 20, 2603–2618.

Lorenzo O, Piqueras R, Sánchez-Serrano J J, Solano R. 2003. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. The Plant Cell15, 165–178.

Lu Q, Niu X, Zhang M, Wang C, Xu Q, Feng Y, Yang Y, Wang S, Yuan X, Yu H, Wang Y, Chen X, Liang X, Wei X. 2018. Genome-wide association study of seed dormancy and the genomic consequences of improvement footprints in rice (Oryza sativa L.). Frontiers in Plant Science8, 2213.

Lu Q, Zhang M, Niu X, Wang S, Xu Q, Feng Y, Wang C, Deng H, Yuan X, Yu H, Wang Y, Wei X. 2015. Genetic variation and association mapping for 12 agronomic traits in indica rice. BMC Genomics, 16, 1067.

Magwa R A, Zhao H, Xing Y. 2016. Genome-wide association mapping revealed a diverse genetic basis of seed dormancy across subpopulations in rice (Oryza sativa L.). BMC Genetics17, 28.

Mather K A, Caicedo A L, Polato N R, Olsen K M, McCouch S, Purugganan M D. 2007. The extent of linkage disequilibrium in rice (Oryza sativa L.). Genetics, 177, 2223–2232.

McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, DePristo M A. 2010. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research20, 1297–1303.

Miao C, Wang Z, Zhang L, Yao J, Hua K, Liu X, Shi H, Zhu J K. 2019. The grain yield modulator miR156 regulates seed dormancy through the gibberellin pathway in rice. Nature Communication, 103822.

Miyamoto T, Takada R, Tobimatsu Y, Suzuki S, Yamamura M, Osakabe K, Osakabe Y, Sakamoto M, Umezawa T. 2020. Double knockout of OsWRKY36 and OsWRKY102 boosts lignification with altering culm morphology of rice. Plant Science, 296110466.

Mohanty B, Takahashi H, de Los Reyes B G, Wijaya E, Nakazono M, Lee D Y. 2016. Transcriptional regulatory mechanism of alcohol dehydrogenase 1-deficient mutant of rice for cell survival under complete submergence. Rice9, 51.

Müller M, Munné-Bosch S. 2015. Ethylene response factors: A key regulatory hub in hormone and stress signaling. Plant Physiology169, 32–41.

Nonogaki H, Barrero J M, Li C. 2018. Editorial: Seed dormancy, germination, and pre-harvest sprouting. Frontiers in Plant Science9, 1783.

Nonogaki M, Nonogaki H. 2017. Prevention of preharvest sprouting through hormone engineering and germination recovery by chemical biology. Frontiers in Plant Science890.

Oracz K, El-Maarouf-Bouteau H, Bogatek R, Corbineau F, Bailly C. 2008. Release of sunflower seed dormancy by cyanide: Cross-talk with ethylene signalling pathway. Journal of Experimental Botany59, 2241–2251.

Park M, Choi W, Shin S Y, Moon H, Lee D, Gho Y S, Jung K H, Jeon J S, Shin C. 2021. Identification of genes and microRNAs affecting pre-harvest sprouting in rice (Oryza sativa L.) by transcriptome and small RNAome analyses. Frontiers in Plant Science121677.

Phitaktansakul R, Kim K W, Aung K M, Maung T Z, Min M H, Somsri A, Lee W, Lee S B, Nam J, Kim S H, Lee J, Kwon S K, Nawade B, Chu S H, Park S W, Kang K K, Cho Y H, Lee Y S, Chung I M, Park Y J. 2022. Multi-omics analysis reveals the genetic basis of rice fragrance mediated by betaine aldehyde dehydrogenase 2Journal of Advanced Research42, 303–314.

Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira M A, Bender D, Maller J, Sklar P, De Bakker P I, Daly M J. 2007. PLINK: A tool set for whole-genome association and population-based linkage analyses. The American Journal of Human Genetics81, 559–575.

Raj A, Stephens M, Pritchard J K. 2014. fastSTRUCTURE: Variational inference of population structure in large SNP data sets. Genetics197, 573–589.

Rashid M, He G Y, Yang G X, Hussain J, Yan X. 2012. AP2/ERF transcription factor in rice: Genome-wide canvas and syntenic relationships between monocots and eudicots. Evolutionary Bioinformatics8, 321–355.

Rodríguez M V, Barrero J M, Corbineau F, Gubler F, Benech-Arnold R L. 2015. Dormancy in cereals (not too much, not so little): About the mechanisms behind this trait. Seed Science Research, 25, 99–119.

Rozas J, Ferrer-Mata A, Sánchez-DelBarrio J C, Guirao-Rico S, Librado P, Ramos-Onsins S E, Sánchez-Gracia A. 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34, 3299–3302.

Shu K, Meng Y J, Shuai H W, Liu W G, Du J B, Liu J, Yang W Y. 2015. Dormancy and germination: How does the crop seed decide? Plant Biology, 17, 1104–1112.

Sohn S I, Pandian S, Kumar T S, Zoclanclounon Y A B, Muthuramalingam P, Shilpha J, Satish L, Ramesh M. 2021. Seed dormancy and pre-harvest sprouting in rice - An updated overview. International Journal of Molecular Sciences, 22, 11804.

Song S, Wang G, Wu H, Fan H, Liang L, Zhao H, Li S, Hu Y, Liu H, Ayyad M, Xing Y, 2020. OsMFT2 is involved in the regulation of ABA signaling-mediated seed germination through interacting with OsbZIP23/66/72 in rice. The Plant Journal, 103, 532–546.

Stagnati L, Lanubile A, Samayoa L F, Bragalanti M, Giorni P, Busconi M, Holland J B, Marocco A. 2019. A genome-wide association study reveals markers and genes associated with resistance to Fusarium verticillioides infection of seedlings in a maize diversity panel. G39, 571–579.

Sugimoto K, Takeuchi Y, Ebana K, Miyao A, Hirochika H, Hara N, Ishiyama K, Kobayashi M, Ban Y, Hattori T, Yano M. 2010. Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proceedings of the National Academy of Sciences of the United States of America107, 5792–5797.

Sweeney M T, Thomson M J, Pfeil B E, McCouch S. 2006. Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. The Plant Cell18, 283–294.

Tai L, Wang H J, Xu X J, Sun W H, Ju L, Liu W T, Li W Q, Sun J, Chen K M. 2021. Pre-harvest sprouting in cereals: Genetic and biochemical mechanisms. Journal of Experimental Botany72, 2857–2876.

Toolkit P. 2019. Broad institute, GitHub repository. [2022-12-22]. http://broadinstitute.github.io/picard

Upadhyaya H D, Wang Y H, Sastry D V, Dwivedi S L, Prasad P V, Burrell A M, Klein R R, Morris G P, Klein P E. 2016. Association mapping of germinability and seedling vigor in sorghum under controlled low-temperature conditions. Genome, 59, 137–145.

Varshney R K, Bohra A, Yu J, Graner A, Zhang Q, Sorrells M E. 2021. Designing future crops: Genomics-assisted breeding comes of age. Trends in Plant Science, 26, 631–649.

Wang H, Zhang Y, Xiao N, Zhang G, Wang F, Chen X, Fang R. 2020. Rice GERMIN-LIKE PROTEIN 2–1 functions in seed dormancy under the control of abscisic acid and gibberellic acid signaling pathways. Plant Physiology, 1831157–1170.

Wickham H, Chang W, Wickham M H. 2016. Package ‘ggplot2’. Create elegant data visualisations using the grammar of graphics. Version, 2, 1–189.

Wilson R L, Kim H, Bakshi A, Binder B M. 2014. The ethylene receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 have contrasting roles in seed germination of Arabidopsis during salt stress. Plant Physiology, 165, 1353–1366.

Wing R A, Purugganan M D, Zhang Q. 2018. The rice genome revolution: From an ancient grain to Green Super Rice. Nature Reviews Genetics19, 505–517.

Xu F, Tang J, Gao S, Cheng X, Du L, Chu C. 2019. Control of rice pre-harvest sprouting by glutaredoxin-mediated abscisic acid signaling. Plant Journal100, 1036–1051.

Xu F, Tang J, Wang S, Cheng X, Wang H, Ou S, Gao S, Li B, Qian Y, Gao C, Chu C. 2022. Antagonistic control of seed dormancy in rice by two bHLH transcription factors. Nature Genetics, 54, 1972–1982.

Xu H, Gao Y, Wang J. 2012. Transcriptomic analysis of rice (Oryza sativa) developing embryos using the RNA-Seq technique. PLoS ONE, 7, e30646.

Xu S, Wang L, Zhang B, Han B, Xie Y, Yang J, Zhong W, Chen H, Wang R, Wang N, Cui W, Shen W. 2012. RNAi knockdown of rice SE5 gene is sensitive to the herbicide methyl viologen by the down-regulation of antioxidant defense. Plant Molecular Biology80, 219–235.

Yang C, Lu X, Ma B, Chen S Y, Zhang J S. 2015. Ethylene signaling in rice and Arabidopsis: Conserved and diverged aspects. Molecular Plant8, 495–505.

Yang J, Lee S H, Goddard M E, Visscher P M. 2011. GCTA: A tool for genome-wide complex trait analysis. American Journal of Human Genetics88, 76–82.

Zhang C, Zhou L, Lu Y, Yang Y, Feng L, Hao W, Li Q, Fan X, Zhao D, Liu Q. 2020. Changes in the physicochemical properties and starch structures of rice grains upon pre-harvest sprouting. Carbohydrate Polymers, 234, 115893.

Zhang Z, Ersoz E, Lai C Q, Todhunter R J, Tiwari H K, Gore M A, Bradbury P J, Yu J, Arnett D K, Ordovas J M, Buckler E S. 2010. Mixed linear model approach adapted for genome-wide association studies. Nature Genetics42, 355–360.

Zhao B, Zhang H, Chen T, Ding L, Zhang L, Ding X, Zhang J, Qian Q, Xiang Y. 2022. Sdr4 dominates pre-harvest sprouting and facilitates adaptation to local climatic condition in Asian cultivated rice. Journal of Integrative Plant Biology64, 1246–1263.

Zhao H, Li J, Yang L, Qin G, Xia C, Xu X, Su Y, Liu Y, Ming L, Chen L L, Xiong L, Xie W. 2021. An inferred functional impact map of genetic variants in rice. Molecular Plant14, 1584–1599.

Zhou C, Lin Q, Lan J, Zhang T, Liu X, Miao R, Mou C, Nguyen T, Wang J, Zhang X, Zhou L, Zhu X, Wang Q, Zhang X, Guo X, Liu S, Jiang L, Wan J. 2020. WRKY transcription factor OsWRKY29 represses seed dormancy in rice by weakening abscisic acid response. Frontiers Plant Science11, 691.

Zhou Q, Wang Q, Ye S, Cui M, Lei W, Gao H, Zhao Y, Xu X, Tang Z, Li J, Cui C. 2019. Genome-wide association analysis of tribenuron-methyl tolerance related traits in Brassica napus L. under germination. Scientia Agricultura Sinica5, 399–413. (in Chinese)

Zhu D, Qian Z, Wei H, Guo B, Xu K, Dai Q, Zhang H, Huo Z. 2019. The effects of field pre-harvest sprouting on the morphological structure and physicochemical properties of rice (Oryza sativa L.) starch. Food Chemistry278, 10–16.

[1] Chengwei Huang, Zhijuan Ji, Qianqian Huang, Liling Peng, Wenwen Li, Dandan Wang, Zepeng Wu, Jia Zhao, Yongqi He, Zhoufei Wang. Natural variation in the cytochrome c oxidase subunit 5B OsCOX5B regulates seed vigor by altering energy production in rice[J]. >Journal of Integrative Agriculture, 2024, 23(9): 2898-2910.
[2] Xinrui Li, Xiafei Li, Tao Liu, Huilai Yin, Hao Fu, Yongheng Luo, Yanfu Bai, Hongkun Yang, Zhiyuan Yang, Yongjian Sun, Jun Ma, Zongkui Chen. Strategies for improving crop comprehensive benefits via a decision-making system based on machine learning in the rice‒rape, rice‒wheat and rice‒garlic rotation systems in Southwest China[J]. >Journal of Integrative Agriculture, 2024, 23(9): 2970-2988.
[3] Zijuan Ding, Ren Hu, Yuxian Cao, Jintao Li, Dakang Xiao, Jun Hou, Xuexia Wang. Integrated assessment of yield, nitrogen use efficiency and ecosystem economic benefits of use of controlled-release and common urea in ratoon rice production[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3186-3199.
[4] Delei Kong, Xianduo Zhang, Qidong Yu, Yaguo Jin, Peikun Jiang, Shuang Wu, Shuwei Liu, Jianwen Zou. Mitigation of N2O emissions in water-saving paddy fields: Evaluating organic fertilizer substitution and microbial mechanisms[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3159-3173.
[5] Xue Shen, Quanyu Yang, Rongjun Ao, Shengsheng Gong. Rural labor migration and farmers’ arrangements of rice production systems in Central China: Insight from the intergenerational division of labor[J]. >Journal of Integrative Agriculture, 2024, 23(9): 3200-3214.
[6] Peng Xu, Mengdie Jiang, Imran Khan, Muhammad Shaaban, Hongtao Wu, Barthelemy Harerimana, Ronggui Hu. Regulatory potential of soil available carbon, nitrogen, and functional genes on N2O emissions in two upland plantation systems[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2792-2806.
[7] Gaozhao Wu, Xingyu Chen, Yuguang Zang, Ying Ye, Xiaoqing Qian, Weiyang Zhang, Hao Zhang, Lijun Liu, Zujian Zhang, Zhiqin Wang, Junfei Gu, Jianchang Yang. An optimized strategy of nitrogen-split application based on the leaf positional differences in chlorophyll meter readings[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2605-2617.
[8] Xiaogang He, Zirong Li, Sicheng Guo, Xingfei Zheng, Chunhai Liu, Zijie Liu, Yongxin Li, Zheming Yuan, Lanzhi Li. Epistasis-aware genome-wide association studies provide insights into the efficient breeding of high-yield and high-quality rice[J]. >Journal of Integrative Agriculture, 2024, 23(8): 2541-2556.
[9] Bin Lei, Jiale Shao, Feng Zhang, Jian Wang, Yunhua Xiao, Zhijun Cheng, Wenbang Tang, Jianmin Wan. Genetic analysis and fine mapping of a grain size QTL in the small-grain sterile rice line Zhuo201S[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2155-2163.
[10] Hanzhu Gu, Xian Wang, Minhao Zhang, Wenjiang Jing, Hao Wu, Zhilin Xiao, Weiyang Zhang, Junfei Gu, Lijun Liu, Zhiqin Wang, Jianhua Zhang, Jianchang Yang, Hao Zhang.

The response of roots and the rhizosphere environment to integrative cultivation practices in paddy rice [J]. >Journal of Integrative Agriculture, 2024, 23(6): 1879-1896.

[11] Luqi Jia, Yongdong Dai, Ziwei Peng, Zhibo Cui, Xuefei Zhang, Yangyang Li, Weijiang Tian, Guanghua He, Yun Li, Xianchun Sang.

The auxin transporter OsAUX1 regulates tillering in rice (Oryza sativa) [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1454-1467.

[12] Chaoyue Pang, Ling Jin, Haoyu Zang, Damalk Saint-Claire S. Koklannou, Jiazhi Sun, Jiawei Yang, Yongxing Wang, Liang Xu, Chunyan Gu, Yang Sun, Xing Chen, Yu Chen. Establishment of a system for screening and identification of novel bactericide targets in the plant pathogenic bacterium Xanthomonas oryzae pv. oryzae using Tn-seq and SPR[J]. >Journal of Integrative Agriculture, 2024, 23(5): 1580-1592.
[13] Yuguang Zang, Gaozhao Wu, Qiangqiang Li, Yiwen Xu, Mingming Xue, Xingyu Chen, Haiyan Wei, Weiyang Zhang, Hao Zhang, Lijun Liu, Zhiqin Wang, Junfei Gu, Jianchang Yang.

Irrigation regimes modulate non-structural carbohydrate remobilization and improve grain filling in rice (Oryza sativa L.) by regulating starch metabolism [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1507-1522.

[14] Shuang Cheng, Zhipeng Xing, Chao Tian, Mengzhu Liu, Yuan Feng, Hongcheng Zhang.

Optimized tillage methods increase mechanically transplanted rice yield and reduce the greenhouse gas emissions [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1150-1163.

[15] Yunping Chen, Jie Hu, Zhiwen Cai, Jingya Yang, Wei Zhou, Qiong Hu, Cong Wang, Liangzhi You, Baodong Xu.

A phenology-based vegetation index for improving ratoon rice mapping using harmonized Landsat and Sentinel-2 data [J]. >Journal of Integrative Agriculture, 2024, 23(4): 1164-1178.

No Suggested Reading articles found!