Please wait a minute...
Journal of Integrative Agriculture  2026, Vol. 25 Issue (3): 847-863    DOI: 10.1016/j.jia.2024.06.012
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide association study reveals genomic regions for nitrogen, phosphorus and potassium use efficiency in bread wheat

Jili Xu1*, Shuo Liu2*, Zhiyuan Gao1*, Qingdong Zeng3, Xiaowen Zhang1, Dejun Han4#, Hui Tian1#

1 College of Natural Resources and Environment, Northwest A&F University/Key Laboratory of Plant Nutrition and the Agri-environment in Northwest China, Ministry of Agriculture and Rural Affairs, Yangling 712100, China

2 Cultivated Land Quality Protection Station, Lianyungang Agricultural and Rural Bureau, Lianyungang 712100, China

3 State Key Laboratory of Crop Stress Resistance and High-Efficiency Production/College of Plant Protection, Northwest A&F University, Yangling 712100, China

4 State Key Laboratory of Crop Stress Resistance and High-Efficiency Production/College of Agronomy, Northwest A&F University, Yangling 712100, China

 Highlights 
A total of 534 quantitative trait loci (QTLs) were identified though genome-wide association study (GWAS).
Through integrated meta-QTL analysis, QTL80, QTL387, and QTL500 were found to be co-localized quantitative trait loci, while QTL234 was identified as a novel locus.
A dCAPS marker was developed for the SNP (AX-109095537) within the nitrogen harvest index (NHI)-associated QTL234.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

培育氮、磷、钾高效利用的小麦品种是实现农业可持续发展的重要途径。对养分利用效率的关键基因进行遗传解析和鉴定是实现这一目标的理想策略。我们利用431不同小麦品种进行了全基因组关联分析(GWAS),揭示了1659个显著的单核苷酸多态性(SNPs)(LOD>5)。本研究在5个环境中共检测到534个与12个养分利用效率性状相关的数量性状位点(QTLs),其中14QTLs至少在3个环境中被同时检测到。通过meta-QTL分析,发现QTL8072.12~74.24 Mb,chr2A)QTL38732.88~33.56 Mb,chr6A)QTL500535.53-540.80 Mb,chr7B)分别与MQTL-2A-2MQTL-6A-1MQTL-7B-2共定位这种趋同表明这些位点在不同环境条件下显著相关性。在这些区域内,我们找到了与养分利用效率相关的关键候选基因,如bZIP转录因子家族基因和钾转运体基因。此外,我们还发现了一个新位点QTL234此区域包含dof锌指蛋白、Ankyrin重复家族蛋白、细胞色素P450等关键候选基因。为了验证与氮收获指数相关的位于QTL234内的一个重要SNP,我们开发了这个位点(AX-109095537dCAPS标记。这些发现表明基于高分辨率SNPGWAS在快速识别潜在关键候选基因方面的有效性为大规模QTL精细定位、候选基因验证和功能标记的开发奠定了基础。此外,本研究鉴定出氮、磷、钾利用效率相关性状的候选基因,并开发了重要SNP的分子标记,对推进小麦养分利用效率育种进程具有重要意义



Abstract  

The development of wheat cultivars with improved nitrogen (N), phosphorus (P), and potassium (K) use efficiency is essential for sustainable agriculture.  Genetic dissection and identification of causative genes underlying nutrient use efficiency represent a key strategy toward this goal.  We conducted an extensive genome-wide association study (GWAS) using a panel of 431 wheat cultivars, identifying 1,659 significant single-nucleotide polymorphisms (SNPs) (LOD>5) through genotyping-by-sequencing.  This analysis revealed 534 quantitative trait loci (QTLs) associated with 12 nutrient use efficiency traits across five distinct environments, among which 14 QTLs were consistently detected in at least three environments.  Notably, meta-QTL analysis, showed that QTL80 (72.12–74.24 Mb, chr2A), QTL387 (32.88–33.56 Mb, chr6A), and QTL500 (535.53–540.80 Mb, chr7B) exhibit clear co-localization with MQTL-2A-2, MQTL-6A-1, and MQTL-7B-2, respectively.  This overlap highlights their robustness across diverse environmental conditions.  Within these regions, critical candidate genes - including members of the bZIP transcription factor family and a potassium transporter gene - were identified in relation to nutrient use efficiency.  Furthermore, a novel locus, QTL234, was discovered, harboring key candidate genes such as dof zinc finger protein, Ankyrin repeat family protein, and cytochrome P450.  To validate the SNP within QTL234 associated with nitrogen harvest index (NHI), we developed a dCAPS marker for AX-109095537.  These findings demonstrate the effectiveness of high-resolution SNP-based GWAS in rapidly pinpointing promising candidate genes.  They also establish a foundation for large-scale QTL fine mapping, candidate gene validation, and the development of functional markers essential for enhancing nutrient use efficiency in wheat breeding programs.


Keywords:  wheat       genome-wide association        nutrient use efficiency        meta-QTL analysis        candidate genes  
Received: 24 February 2024   Accepted: 06 May 2024 Online: 27 June 2024  
Fund: The work was funded by the National Key R&D Program of China (2021YFD1900700).  
About author:  Jili Xu, E-mail: 2021060380@nwafu.edu.cn; Shuo Liu, E-mail: 732361104@qq.com; Zhiyuan Gao, E-mail: 739162009@qq.com; #Correspondence Dejun Han, E-mail: handj@nwsuaf.edu.cn; Hui Tian, E-mail: tianh@nwsuaf.edu.cn

Cite this article: 

Jili Xu, Shuo Liu, Zhiyuan Gao, Qingdong Zeng, Xiaowen Zhang, Dejun Han, Hui Tian. 2026. Genome-wide association study reveals genomic regions for nitrogen, phosphorus and potassium use efficiency in bread wheat. Journal of Integrative Agriculture, 25(3): 847-863.

Alemu G, Dabi A, Geleta N, Duga R, Solomon T, Zegaye H, Getamesay A, Delesa A, Asnake D, Asefa B, Shewaye Y, Abeyo B G, Badebo A. 2021. Genotype×environment interaction and selection of high yielding wheat genotypes for different wheat-growing areas of Ethiopia. American Journal of BioScience9, 63–71.

Arcade A, Labourdette A, Falque M, Mangin B, Chardon F, Charcosset A, Joets J. 2004. BioMercator: integrating genetic maps and QTL towards discovery of candidate genes. Bioinformatics20, 2324–2326.

Arjona J M, Royo C, Dreisigacker S, Ammar K, Villegas D. 2018. Effect of Ppd-A1 and Ppd-B1 allelic variants on grain number and thousand kernel weight of durum wheat and their impact on final grain yield. Frontiers in Plant Science9, 888.

Bandyopadhyay T, Swarbreck S M, Jaiswal V, Maurya J, Gupta R, Bentley A R, Griffiths H, Prasad M. 2022. GWAS identifies genetic loci underlying nitrogen responsiveness in the climate resilient C4 model Setaria italica (L.). Journal of Advanced Research42, 249–261.

Barraclough P B, Howarth J R, Jones J, Lopez-Bellido R, Parmar S, Shepherd C E, Hawkesford M J. 2010. Nitrogen efficiency of wheat: Genotypic and environmental variation and prospects for improvement. European Journal of Agronomy33, 1–11.

Brasier K, Ward B, Smith J, Seago J, Oakes J, Balota M, Davis P, Fountain M, Brown-Guedira G, Sneller C, Thomason W, Griffey C. 2020. Identification of quantitative trait loci associated with nitrogen use efficiency in winter wheat. PLoS ONE15, e0228775.

Chai L, Xin M, Dong C, Chen Z, Zhai H, Zhuang J, Cheng X, Wang N, Geng J, Wang X, Bian R, Yao Y, Guo W, Hu Z, Peng H, Bai G, Sun Q, Su Z, Liu J, Ni Z. 2022. A natural variation in Ribonuclease H-like gene underlies Rht8 to confer “Green Revolution” trait in wheat. Molecular Plant15, 377–380.

Chen Q, Guo Z R, Shi X L, Wei M Q, Fan Y Z, Zhu J, Zheng T, Wang Y, Kong L, Deng M, Cao X Y, Wang J R, Wei Y M, Jiang Q T, Jiang Y F, Chen G Y, Zheng Y L, Qi P F. 2022. Increasing the grain yield and grain protein content of common wheat (Triticum aestivum) by introducing missense mutations in the Q gene. International Journal of Molecular Sciences23, 10772.

Cheng X Y, Liu X D, Mao W W, Zhang X R, Chen S L, Zhan K H, Bi H H, Xu H X. 2018. Genome-wide identification and analysis of HAK/KUP/KT potassium transporters gene family in wheat (Triticum aestivum L.). International Journal of Molecular Sciences19, 3969.

Cormier F, Le Gouis J, Dubreuil P, Lafarge S, Praud S. 2014. A genome-wide identification of chromosomal regions determining nitrogen use efficiency components in wheat (Triticum aestivum L.). Theoretical and Applied Genetics127, 2679–2693.

Cui F, Fan X, Zhao C, Zhang W, Chen M, Ji J, Li J. 2014. A novel genetic map of wheat: Utility for mapping QTL for yield under different nitrogen treatments. BMC Genetics15, 57.

Darvasi A, Soller M. 1997. A simple method to calculate resolving power and confidence interval of QTL map location. Behavior Genetics27, 125–132.

Darzi-Ramandi H, Shariati V J, Tavakol E, Najafi-Zarini H, Bilgrami S S, Razavi K. 2017. Detection of consensus genomic regions associated with root architecture of bread wheat on groups 2 and 3 chromosomes using QTL meta-analysis. Australian Journal of Crop Science111, 777–785.

Duan X, Yu H, Ma W, Sun J, Zhao Y, Yang R, Ning T, Li Q, Liu Q, Guo T, Yan M, Tian J, Chen J. 2020. A major and stable QTL controlling wheat thousand grain weight: Identification, characterization, and CAPS marker development. Molecular Breeding40, 68.

Earl D A, Vonholdt B M. 2012. STRUCTURE HARVESTER: A website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources4, 359–361.

Forthoffer N, Helvig C, Dillon N, Benveniste I, Zimmerlin A, Tardif F, Salaun J P. 2001. Induction and inactivation of a cytochrome P450 confering herbicide resistance in wheat seedlings. European Journal of Drug Metabolism and Pharmacokinetics26, 9–16.

Frels K, Guttieri M, Joyce B, Leavitt B, Baenziger P S. 2018. Evaluating canopy spectral reflectance vegetation indices to estimate nitrogen use traits in hard winter wheat. Field Crops Research217, 82–92.

Gaju O, DeSilva J, Carvalho P, Hawkesford M J, Griffiths S, Greenland A, Foulkes M J. 2016. Leaf photosynthesis and associations with grain yield, biomass and nitrogen-use efficiency in landraces, synthetic-derived lines and cultivars in wheat. Field Crops Research193, 1–15.

Giordano N, Sadras V O, Lollato R P. 2023. Late-season nitrogen application increases grain protein concentration and is neutral for yield in wheat. A global meta-analysis. Field Crops Research290, 108740.

Górny A G, Banaszak Z, Ługowska B, Ratajczak D. 2011. Inheritance of the efficiency of nitrogen uptake and utilization in winter wheat (Triticum aestivum L.) under diverse nutrition levels. Euphytica, 177, 191–206.

Guo B, Sleper D A, Lu P, Shannon J G, Nguyen H T, Arelli P R. 2006. QTLs associated with resistance to soybean cyst nematode in soybean meta-analysis of QTL locations - Retraction. Crop Science46, 595–602.

Guo Y, Kong F M, Xu Y F, Zhao Y, Liang X, Wang Y Y, An D G, Li S S. 2012. QTL mapping for seedling traits in wheat grown under varying concentrations of N, P and K nutrients. Theoretical and Applied Genetics, 124, 851–865.

Guo Y, Sun J, Zhang G, Wang Y, Kong F, Zhao Y, Li S. 2013. Haplotype, molecular marker and phenotype effects associated with mineral nutrient and grain size traits of TaGS1a in wheat. Field Crops Research154, 119–125.

Guttieri M J, Frels K, Regassa T, Waters B M, Baenziger P S. 2017. Variation for nitrogen use efficiency traits in current and historical great plains hard winter wheat. Euphytica213, 87.

Han X, Zhang M, Gao M, Yuan Y, Yuan Y, Zhang G, An Y, Guo Y, Kong F, Li S. 2023. QTL mapping and candidate gene identifying for N, P, and K use efficiency at the maturity stages in wheat. Genes14, 1168.

Hao T, Zhu Q, Zeng M, Shen J, Shi X, Liu X, Zhang F, de Vries W. 2020. Impacts of nitrogen fertilizer type and application rate on soil acidification rate under a wheat–maize double cropping system. Journal of Environmental Management270, 110888.

Hao Y C, Kong F M, Wang L L, Zhao Y, Li M Y, Che N X, Li S, Wang M, Hao M, Zhang X C, Zhao Y. 2024. Genome-wide association study of grain micronutrient concentrations in bread wheat. Journal of Integrative Agriculture23, 1468–1480.

Hawkesford M J. 2017. Genetic variation in traits for nitrogen use efficiency in wheat. Journal of Experimental Botany68, 2627–2632.

He W S. 2003. Genotypic differences in phosphorus utilization efficiency among spring wheat varieties in Ningxia. Agricultural Research in the Arid Areas2, 1–6. (in Chinese)

Huang J F, Li L, Mao X G, Wang J Y, Liu H M, Li C N, Jing R L. 2020. dCAPS markers developed for nitrate transporter genes TaNRT2L12s associating with 1 000-grain weight in wheat. Journal of Integrative Agriculture, 19, 1543–1553.

Jing F, Miao Y, Zhang P, Chen T, Liu Y, Ma J, Li M, Yang D. 2022. Characterization of TaSPP-5A gene associated with sucrose content in wheat (Triticum aestivum L.). BMC Plant Biology22, 58.

Kolodziej M C, Singla J, Sánchez-Martín J, Zbinden H, Šimková H, Karafiátová M, Doležel J, Gronnier J, Poretti M, Glauser G, Zhu W, Köster P, Zipfel C, Wicker T, Krattinger S G, Keller B. 2021. A membrane-bound ankyrin repeat protein confers race-specific leaf rust disease resistance in wheat. Nature Communications, 12, 956.

Kreutz G F, Bhadha J H, Sandoya G V. 2022. Examining phosphorus use efficiency across different lettuce (Lactuca sativa L.) accessions. Euphytica218, 28.

Kusin F M, Akhir N I M, Mohamat-Yusuff F, Awang M. 2015. The impact of nitrogen fertilizer use on greenhouse gas emissions in an oil palm plantation associated with land use change. Atmosfera28, 243–250.

Leip A, Ledgard S F, Uwizeye A, Fusi A, Raffa D W. 2018. Nutrient Flows and associated environmental impacts in livestock supply chains. Guidelines for assessment. version 1. FAO, Food and Agriculture Organization of the United Nations, Rome.

Li M X, Yeung J M, Cherny S S, Sham P C. 2012. Evaluating the effective numbers of independent tests and significant P-value thresholds in commercial genotyping arrays and public imputation reference datasets. Human Genetics131, 747–756.

Li Q, Wang J Y, Khan N, Chang X P, Liu H M, Jing R L. 2016. Polymorphism and association analysis of a drought-resistant gene TaLTP-s in wheat. Journal of Integrative Agriculture15, 1198–1206.

Li X, Zhang J B, Song B, Li H P, Xu H Q, Qu B, Dang F J, Liao Y C. 2010. Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathology100, 183–191.

Liang Z, Bronson K F, Thorp K R, Mon J, Badaruddin M, Wang G. 2014. Cultivar and N fertilizer rate affect yield and N use efficiency in irrigated durum wheat. Crop Science54, 1175–1183.

Lin Y, Chen G, Hu H, Yang X, Zhang Z, Jiang X, Wu F, Shi H, Wang Q, Zhou K, Li C, Ma J, Zheng Y, Wei Y, Liu Y. 2020. Phenotypic and genetic variation in phosphorus-deficiency-tolerance traits in Chinese wheat landraces. BMC Plant Biology20, 330.

Liu H, Wang J, Zhang B, Yang X, Hammond J P, Ding G, Wang S, Cai H, Wang C, Xu F, Shi L. 2021. Genome-wide association study dissects the genetic control of plant height and branch number in response to low-phosphorus stress in Brassica napusAnnals of Botany128, 919–930.

Liu Q, Zhao Y, Rahman S, She M, Zhang J, Yang R, Islam S, O’Hara G, Varshney R K, Liu H, Ma H, Ma W. 2023. The putative vacuolar processing enzyme gene TaVPE3cB is a candidate gene for wheat stem pith-thickness. Theoretical and Applied Genetics136, 138.

Ma Z, He S, Wang X, Sun J, Zhang Y, Zhang G, Wu L, Li Z, Liu Z, Sun G, Yan Y, Jia Y, Yang J, Pan Z, Gu Q, Li X, Sun Z, Dai P, Liu Z, Gong W, et al. 2018. Resequencing a core collection of upland cotton identifies genomic variation and loci influencing fiber quality and yield. Nature Genetics50, 803–813.

Manske G G B, Ortiz-Monasterio J I, van Ginkel M, González R M, Fischer R A, Rajaram S, Vlek P L G. 2001. Importance of P uptake efficiency versus P utilization for wheat yield in acid and calcareous soils in Mexico. European Journal of Agronomy14, 261–274.

McDonald G K, Taylor J D, Gong X, Bovill W. 2018. Responses to phosphorus among barley genotypes. Crop & Pasture Science69, 574–586.

Meier S, Morales A, López-Olivari R, Matus I, Aponte H, Campos P de S, Khan N, Cartes P, Meriño-Gergichevich C, Castillo D, Seguel A. 2022. Synergistic role between phosphorus and water use efficiency in spring wheat genotypes. Agricultural Water Management263, 107481.

Mizutani M, Sato F. 2011. Unusual P450 reactions in plant secondary metabolism. Archives of Biochemistry and Biophysics507, 194–203.

Mueth N A, Hulbert S H. 2022. Small RNAs target native and cross-kingdom transcripts on both sides of the wheat stripe rust interaction. Genomics114, 110526.

Neff M M, Turk E, Kalishman M. 2002. Web-based primer design for single nucleotide polymorphism analysis. Trends in Genetics18, 613–615.

Ober C, Butte A J, Elias J A, Lusis A J, Gan W, Banks-Schlegel S, Schwartz D. 2010. Getting from genes to function in lung disease: A National Heart, Lung, and Blood Institute workshop report. American Journal of Respiratory and Critical Care Medicine182, 732–737.

de Oliveira Silva A, Ciampitti I A, Slafer G A, Lollato R P. 2020. Nitrogen utilization efficiency in wheat: A global perspective. European Journal of Agronomy114, 126008.

Patial N. 2021. Genetic variability studies in germplasm of wheat (Triticum aestivum L.). Annals of Plant and Soil Research23, 310–313.

Peng J, Richards D E, Hartley N M, Murphy G P, Devos K M, Flintham J E, Beales J, Fish L J, Worland A J, Pelica F, Sudhakar D, Christou P, Snape J W, Gale M D, Harberd N P. 1999. ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature400, 256–261.

Pinot F, Alayrac C, Mioskowski C, Durst F, Salaun J P. 1994. New cytochrome P450-dependent reactions from wheat: Terminal and sub-terminal hydroxylation of oleic acid by microsomes from naphthalic acid anhydride and phenobarbital induced wheat seedlings. Biochemical and Biophysical Research Communications198, 795–803.

Quraishi U M, Abrouk M, Murat F, Pont C, Foucrier S, Desmaizieres G, Confolent C, Riviere N, Charmet G, Paux E, Murigneux A, Guerreiro L, Lafarge S, Le Gouis J, Feuillet C, Salse J. 2011. Cross-genome map based dissection of a nitrogen use efficiency ortho-metaQTL in bread wheat unravels concerted cereal genome evolution. Plant Journal65, 745–756.

Rengel Z, Damon P M. 2008. Crops and genotypes differ in efficiency of potassium uptake and use. Physiologia Plantarum133, 624–636.

Safdar L B, Andleeb T, Latif S, Umer M J, Tang M, Li X, Liu S, Quraishi U M. 2020. Genome-wide association study and QTL meta-analysis identified novel genomic loci controlling potassium use efficiency and agronomic traits in bread wheat. Frontiers in Plant Science11, 70.

Safdar L B, Umer M J, Almas F, Uddin S, Safdar Q T, Blighe K, Quraishi U M. 2021. Identification of genetic factors controlling phosphorus utilization efficiency in wheat by genome-wide association study with principal component analysis. Gene768, 145301.

Said J I, Lin Z, Zhang X, Song M, Zhang J. 2013. A comprehensive meta QTL analysis for fiber quality, yield, yield related and morphological traits, drought tolerance, and disease resistance in tetraploid cotton. BMC Genomics14, 776.

Saini D K, Chopra Y, Pal N, Chahal A, Srivastava P, Gupta P K. 2021. Meta-QTLs, ortho-MQTLs and candidate genes for nitrogen use efficiency and root system architecture in bread wheat (Triticum aestivum L.). Physiology and Molecular Biology of Plants27, 2245–2267.

Shi H, Chen M, Gao L, Wang Y, Bai Y, Yan H, Xu C, Zhou Y, Xu Z, Chen J, Tang W, Wang S, Shi Y, Wu Y, Sun D, Jia J, Ma Y. 2022. Genome-wide association study of agronomic traits related to nitrogen use efficiency in wheat. Theoretical and Applied Genetics135, 4289–4302.

Shi H, Wang W, Gao L, Wu J, Hu C, Yan H, Shi Y, Li N, Ma Y, Zhou Y, Xu Z, Chen J, Tang W, Chen K, Sun D, Wu Y, Chen M. 2023. Genome-wide association study of seedling nitrogen-use efficiency-associated traits in common wheat (Triticum aestivum L.). The Crop Journal12, 222–231.

Sosnowski O, Charcosset A, Joets J. 2012. BioMercator V3: An upgrade of genetic map compilation and quantitative trait loci meta-analysis algorithms. Bioinformatics28, 2082–2083.

Soumya P R, Burridge A J, Singh N, Batra R, Pandey R, Kalia S, Rai V, Edwards K J. 2021. Population structure and genome-wide association studies in bread wheat for phosphorus efficiency traits using 35 K Wheat Breeder’s Affymetrix array. Scientific Reports11, 7601.

Su J Y, Zheng Q, Li H W, Li B, Jing R L, Tong Y P, Li Z S. 2009. Detection of QTLs for phosphorus use efficiency in relation to agronomic performance of wheat grown under phosphorus sufficient and limited conditions. Plant Science176, 824–836.

Sun C, Dong Z, Zhao L, Ren Y, Zhang N, Chen F. 2020. The Wheat 660K SNP array demonstrates great potential for marker-assisted selection in polyploid wheat. Plant Biotechnology Journal18, 1354–1360.

Thiemann A, Fu J, Seifert F, Grant-Downton R T, Schrag T A, Pospisil H, Frisch M, Melchinger A E, Scholten S. 2014. Genome-wide meta-analysis of maize heterosis reveals the potential role of additive gene expression at pericentromeric loci. BMC Plant Biology14, 88.

Venske E, Dos Santos R S, Farias D d R, Rother V, da Maia L C, Pegoraro C, Oliveira A C d. 2019. Meta-analysis of the QTLome of Fusarium head blight resistance in bread wheat: Refining the current puzzle. Frontiers in Plant Science10, 727.

Veyrieras J B, Goffinet B, Charcosset A. 2007. MetaQTL: A package of new computational methods for the meta-analysis of QTL mapping experiments. BMC Bioinformatics8, 49.

Vo K T X, Kim C Y, Chandran A K N, Jung K H, An G, Jeon J S. 2015. Molecular insights into the function of ankyrin proteins in plants. Journal of Plant Biology58, 271–284.

Wang L, Liu Y J, Xiao P, Shen H, Deng H Y, Papasian C J, Drees B M, Hamilton J J, Recker R R, Deng H W. 2007. Chromosome 2q32 may harbor a QTL affecting BMD variation at different skeletal sites. Journal of Bone and Mineral Research22, 1672–1678.

Xiong R, He T, Wang Y, Liu S, Gao Y, Yan H, Xiang Y. 2021. Genome and transcriptome analysis to understand the role diversification of cytochrome P450 gene under excess nitrogen treatment. BMC Plant Biology21, 447.

Xu J, Gao Z, Liu S, Elwafa S F A, Tian H. 2022. A multienvironmental evaluation of the N, P and K use efficiency of a large wheat diversity panel. Field Crops Research286, 108634.

Xu Y, Wang R, Tong Y, Zhao H, Xie Q, Liu D, Zhang A, Li B, Xu H, An D. 2014. Mapping QTLs for yield and nitrogen-related traits in wheat: influence of nitrogen and phosphorus fertilization on QTL expression. Theoretical and Applied Genetics127, 59–72.

Yan S N, Yu Z Y, Gao W, Wang X Y, Cao J J, Lu J, Ma C X, Chang C, Zhang H P. 2023. Dissecting the genetic basis of grain color and pre-harvest sprouting resistance in common wheat by association analysis. Journal of Integrative Agriculture22, 2617–2631.

Yang H, Chen R, Chen Y, Li H, Wei T, Xie W, Fan G. 2022. Agronomic and physiological traits associated with genetic improvement of phosphorus use efficiency of wheat grown in a purple lithomorphic soil. The Crop Journal10, 1151–1164.

Yang J, Wang M, Li W, He X, Teng W, Ma W, Zhao X, Hu M, Li H, Zhang Y, Tong Y. 2019. Reducing expression of a nitrate-responsive bZIP transcription factor increases grain yield and N use in wheat. Plant Biotechnology Journal17, 1823–1833.

Yang M J, Wang C R, Hassan M A, Wu Y Y, Xia X C, Shi S B, Xiao Y G, He Z H. 2021. QTL mapping of seedling biomass and root traits under different nitrogen conditions in bread wheat (Triticum aestivum L.). Journal of Integrative Agriculture20, 1180–1192.

Yang S Y, Lin W Y, Hsiao Y M, Chiou T J. 2024. Milestones in understanding transport, sensing, and signaling of the plant nutrient phosphorus. The Plant Cell36, 1–20.

Yang Y, Amo A, Wei D, Chai Y, Zheng J, Qiao P, Cui C, Lu S, Chen L, Hu Y G. 2021. Large-scale integration of meta-QTL and genome-wide association study discovers the genomic regions and candidate genes for yield and yield-related traits in bread wheat. Theoretical and Applied Genetics134, 3083–3109.

Yu S Z, Wu J H, Wang M, Shi W M, Xia G M, Jia J Z, Kang Z S, Han D J. 2020. Haplotype variations in QTL for salt tolerance in Chinese wheat accessions identified by marker-based and pedigree-based kinship analyses. Crop Journal8, 1011–1024.

Zhang L, Zhang L, Xia C, Gao L, Hao C, Zhao G, Jia J, Kong X. 2017. A novel wheat C-bZIP gene, TabZIP14-B, participates in salt and freezing tolerance in transgenic plants. Frontiers in Plant Science, 8, 710.

Zhang L Y, Liu D C, Guo X L, Yang W L, Sun J Z, Wang D W, Zhang A. 2010. Genomic distribution of quantitative trait loci for yield and yield-related traits in common wheat. Journal of Integrative Plant Biology52, 996–1007.

Zhang M, Gao M, Zheng H, Yuan Y, Zhou X, Guo Y, Zhang G, Zhao Y, Kong F, An Y, Li S. 2019. QTL mapping for nitrogen use efficiency and agronomic traits at the seedling and maturity stages in wheat. Molecular Breeding39, 71.

Zhang X, Jia H, Li T, Wu J, Nagarajan R, Lei L, Powers C, Kan C C, Hua W, Liu Z, Chen C, Carver B F, Yan L. 2022. TaCol-B5 modifies spike architecture and enhances grain yield in wheat. Science376, 180–183.

Zhang Y, Zhang G, Xia N, Wang X J, Huang L L, Kang Z S. 2008. Cloning and characterization of a bZIP transcription factor gene in wheat and its expression in response to stripe rust pathogen infection and abiotic stresses. Physiological and Molecular Plant Pathology73, 88–94.

Zhang Z P, Li Z, He F, Lü J J, Xie B, Yi X Y, Li J M, Li J, Song J H, Pu Z E, Ma J, Peng Y Y, Chen G Y, Wei Y M, Zheng Y I, Li W. 2023. Genome-wide association and linkage mapping strategies reveal the genetic loci and candidate genes of important agronomic traits in Sichuan wheat. Journal of Integrative Agriculture22, 3380–3393.

Zhou X, Stephens M. 2012. Genome-wide efficient mixed-model analysis for association studies. Nature Genetics44, 821–824.

[1] Jie Shuai, Qiang Tu, Yicong Zhang, Xiaobo Xia, Yuhua Wang, Shulin Cao, Yifan Dong, Xinli Zhou, Xu Zhang, Zhengguang Zhang, Yi He, Gang Li. Silence of five Fusarium graminearum genes in wheat host confers resistance to Fusarium head blight[J]. >Journal of Integrative Agriculture, 2026, 25(3): 1051-1063.
[2] Shuwei Zhang, Jiajia Zhao, Haiyan Zhang, Duoduo Fu, Ling Qiao, Bangbang Wu, Xiaohua Li, Yuqiong Hao, Xingwei Zheng, Zhen Liang, Zhijian Chang, Jun Zheng. Structural chromosome variations from Jinmai 47 and Jinmai 84 affected agronomic traits and drought tolerance of wheat[J]. >Journal of Integrative Agriculture, 2026, 25(3): 864-878.
[3] Yuhuai Liu, Heng Wang, Li Wang, Jina Ding, Hui Zhai, Qiujin Ma, Can Hu, Tida Ge. Microplastics reduce the wheat (Triticum aestivum L.) net photosynthetic rate through rhizospheric effects[J]. >Journal of Integrative Agriculture, 2026, 25(3): 1263-1275.
[4] Lin Wang, Fei Liu, Yumeng Bian, Mudi Sun, Zhensheng Kang, Jie Zhao. Revealing inheritance of a Xinjiang isolate BGTB-1 of Puccinia striiformis f. sp. tritici and the shift of pathogenicity from avirulence to virulence at heterozygous AvrYr5 locus[J]. >Journal of Integrative Agriculture, 2026, 25(2): 744-755.
[5] Dili Lai, Md. Nurul Huda, Yawen Xiao, Tanzim Jahan, Wei Li, Yuqi He, Kaixuan Zhang, Jianping Cheng, Jingjun Ruan, Meiliang Zhou. Evolutionary and expression analysis of sugar transporters from Tartary buckwheat revealed the potential function of FtERD23 in drought stress[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3334-3350.
[6] Tiantian Chen, Lei Li, Dan Liu, Yubing Tian, Lingli Li, Jianqi Zeng, Awais Rasheed, Shuanghe Cao, Xianchun Xia, Zhonghu He, Jindong Liu, Yong Zhang. Genome wide linkage mapping for black point resistance in a recombinant inbred line population of Zhongmai 578 and Jimai 22[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3311-3321.
[7] Zimeng Liang, Juan Li, Jingyi Feng, Zhiyuan Li, Vinay Nangia, Fei Mo, Yang Liu. Brassinosteroids improve the redox state of wheat florets under low-nitrogen stress and alleviate degeneration[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2920-2939.
[8] Qing Li, Zhuangzhuang Sun, Zihan Jing, Xiao Wang, Chuan Zhong, Wenliang Wan, Maguje Masa Malko, Linfeng Xu, Zhaofeng Li, Qin Zhou, Jian Cai, Yingxin Zhong, Mei Huang, Dong Jiang. Time-course transcriptomic information reveals the mechanisms of improved drought tolerance by drought priming in wheat[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2902-2919.
[9] Liulong Li, Zhiqiang Mao, Pei Wang, Jian Cai, Qin Zhou, Yingxin Zhong, Dong Jiang, Xiao Wang. Drought priming enhances wheat grain starch and protein quality under drought stress during grain filling[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2888-2901.
[10] Xinhu Guo, Jinpeng Chu, Yifan Hua, Yuanjie Dong, Feina Zheng, Mingrong He, Xinglong Dai. Long-term integrated agronomic optimization maximizes soil quality and synergistically improves wheat yield and nitrogen use efficiency[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2940-2953.
[11] Jinpeng Li, Siqi Wang, Zhongwei Li, Kaiyi Xing, Xuefeng Tao, Zhimin Wang, Yinghua Zhang, Chunsheng Yao, Jincai Li. Effects of micro-sprinkler irrigation and topsoil compaction on winter wheat grain yield and water use efficiency in the Huaibei Plain, China[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2974-2988.
[12] Baohua Liu, Ganqiong Li, Yongen Zhang, Ling Zhang, Dianjun Lu, Peng Yan, Shanchao Yue, Gerrit Hoogenboom, Qingfeng Meng, Xinping Chen. Optimizing management strategies to enhance wheat productivity in the North China Plain under climate change[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2989-3003.
[13] Ziqiang Che, Shuting Bie, Rongrong Wang, Yilin Ma, Yaoyuan Zhang, Fangfang He, Guiying Jiang. Mild deficit irrigation delays flag leaf senescence and increases yield in drip-irrigated spring wheat by regulating endogenous hormones[J]. >Journal of Integrative Agriculture, 2025, 24(8): 2954-2973.
[14] Xianhong Zhang, Zhiling Wang, Danmei Gao, Yaping Duan, Xin Li, Xingang Zhou. Wheat cover crop accelerates the decomposition of cucumber root litter by altering the soil microbial community[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2857-2868.
[15] Zhongwei Tian, Yanyu Yin, Bowen Li, Kaitai Zhong, Xiaoxue Liu, Dong Jiang, Weixing Cao, Tingbo Dai. Optimizing planting density and nitrogen application to mitigate yield loss and improve grain quality of late-sown wheat under rice–wheat rotation[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2558-2574.
No Suggested Reading articles found!