Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (4): 1134-1149    DOI: 10.1016/j.jia.2023.05.002
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |

Genome-wide and candidate gene association studies identify BnPAP17 as conferring the utilization of organic phosphorus in oilseed rape

Ping Xu1*, Hao Li2*, Haiyuan Li1, Ge Zhao1, Shengjie Dai1, Xiaoyu Cui1, Zhenning Liu1, Lei Shi2#, Xiaohua Wang1#

1 College of Agriculture and Forestry Science, Linyi University, Linyi 27600, China 2 National Key Laboratory of Crop Genetic Improvement/Microelement Research Centre/Key Laboratory of Arable Land Conservation (Middle and Lower Reaches of Yangtze River), Ministry of Agriculture and Rural Affairs/Huazhong Agricultural University, Wuhan 430070, China 

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

磷(P)是活体植物必不可少的重要元素。缺磷是制约世界油菜产量的关键因素之一。作为植物最重要的器官,根的形态在磷的吸收中起着关键作用。为了研究低磷有效性下根形态的遗传变异性,我们通过全基因组关联研究(GWAS)、连锁作图和候选基因关联研究(CGAS)对跟的形态性状相关的基因结构进行了剖析。在405份油菜自然群体中,共检测到52个重要的标记位点与磷胁迫下的根系形态性状相关。其中,在低磷胁迫下的侧根数(LRN)和根干重(RDW)性状位点中共同检测到紫色酸性磷酸酶基因-BnPAP17。在低磷胁迫下,高效磷品种的地上部组织中BnPAP17的表达比根组织和低效磷品种的表达增加。此外,还检测到BnPAP17Hap3单倍型在油菜磷高效育种中受到了选择。过量表达该单倍型能显著促进油菜的地上部和根部生长,增强油菜对低磷胁迫的耐受性和对有机磷的利用。综上所述,这些发现增加了我们对BnPAP17在介导油菜低磷胁迫中的分子机制的认识。



Abstract  

Phosphorus (P) is essential for living plants, and P deficiency is one of the key factors limiting the yield in rapeseed production worldwide.  As the most important organ for plants, root morphology traits (RMTs) play a key role in P absorption.  To investigate the genetic variability of RMT under low P availability, we dissected the genetic structure of RMTs by genome-wide association studies (GWAS), linkage mapping and candidate gene association studies (CGAS).  A total of 52 suggestive loci were associated with RMTs under P stress conditions in 405 oilseed rape accessions.  The purple acid phosphatase gene BnPAP17 was found to control the lateral root number (LRN) and root dry weight (RDW) under low P stress.  The expression of BnPAP17 was increased in shoot tissue in P-efficient cultivars compared to root tissue and P-inefficient cultivars in response to low P stress.  Moreover, the haplotype of BnPAP17Hap3 was detected for the selective breeding of P efficiency in oilseed rape.  Over-expression of the BnPAP17Hap3 could promote the shoot and root growth with enhanced tolerance to low P stress and organic phosphorus (Po) utilization in oilseed rape.  Collectively, these findings increase our understanding of the mechanisms underlying BnPAP17-mediated low P stress tolerance in oilseed rape.

Keywords:  genome-wide association studies (GWAS)        root morphology traits (RMTs)        organic phosphorus (Po)        oilseed rape        BnPAP17   
Received: 08 February 2023   Online: 10 April 2023   Accepted:
Fund: 

The authors thank Martin R. Broadley from Nottingham University, UK for offering the HTP system and the greenhouse.  This work was financially supported by the National Natural Science Foundation of China (32201868 and 32001575).

About author:  #Correspondence Xiaohua Wang, Tel: +86-539-7258721, E-mail: wangxiaohua19880721@126.com; Lei Shi, E-mail: leish@mail.hzau.edu.cn * These authors contributed equally to this study.

Cite this article: 

Ping Xu, Hao Li, Haiyuan Li, Ge Zhao, Shengjie Dai, Xiaoyu Cui, Zhenning Liu, Lei Shi, Xiaohua Wang. 2024.

Genome-wide and candidate gene association studies identify BnPAP17 as conferring the utilization of organic phosphorus in oilseed rape . Journal of Integrative Agriculture, 23(4): 1134-1149.

Alcock T D, Havlickova L, He Z, Bancroft I, White P J, Broadley M R, Graham N S. 2017. Identification of candidate genes for calcium and magnesium accumulation in Brassica napus L. by association genetics. Frontiers in Plant Science, 8, 1968.

Chalhoub B, Denoeud F, Liu S, Parkin I A, Tang H, Wang X, Chiquet J, Belcram H, Tong C, Samans B, Corréa M, Da Silva C, Just J, Falentin C, Koh C S, Le Clainche I, Bernard M, Bento P, Noel B, Labadie K, et al. 2014. Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science, 345, 950–953.

Deng S, Lu L, Li J, Du Z, Liu T, Li W, Xu F, Shi L, Shou H, Wang C. 2020. Purple acid phosphatase 10c encodes a major acid phosphatase that regulates plant growth under phosphate-deficient conditions in rice. Journal of Experimental Botany, 71, 14.

Du H, Yang C, Ding G, Shi L, Xu F. 2017. Genome-wide identification and characterization of SPX domain-containing members and their responses to phosphate deficiency in Brassica napus. Frontiers in Plant Science, 8, 35.

Evanno G, Regnaut S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE, a simulation study. Molecular Ecology, 14, 2611–2620.

Gahoonia T S, Nielsen N E. 2004. Barley genotypes with long root hairs sustain high grain yields in low-P field. Plant and Soil, 262, 55–62.

Ghahremani M, Park J, Anderson E M, Marty-Howard N J, Mullen R T, Plaxton W C. 2019. Lectin AtGAL1 interacts with high-mannose glycoform of the purple acid phosphatase AtPAP26 secreted by phosphate-starved Arabidopsis. Plant Cell and Environment, 42, 1158–1166.

Haling R E, Brown L K, Bengough A G, Young I M, Hallett P D, White P J, George T S. 2013. Root hairs improve root penetration, root–soil contact, and phosphorus acquisition in soils of different strength. Journal of Experimental Botany, 64, 3711–3721.

Hammond J P, Broadley M R, White P J, King G J, Bowen H C, Hayden R, Meacham M C, Mead A, Overs T, Spracklen W P, Greenwood D J. 2009. Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. Journal of Experimental Botany, 60, 1953–1968.

Hufnagel B, Sousa S M D, Assis L, Guimaraes C T, Leiser W, Azevedo G C, Negri B, Larson B G, Shaff J E, Pastina M M, Barros B A, Weltzien E, Rattunde H F W, Viana J H, Clark R T, Falcão A, Gazaffi R, Augusto A, Garcia F, Schaffert R E, et al. 2014. Duplicate and conquer, multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiology, 166, 659–677.

Hurley B A, Tran H T, Marty N J, Park J, Snedden W A, Mullen R T, Plaxton W C. 2010. The dual-targeted purple acid phosphatase isozyme AtPAP26 is essential for efficient acclimation of Arabidopsis to nutritional phosphate deprivation. Plant Physiology, 153, 1112–1122.

Kaida R, Satoh Y, Bulone V, Yamada Y, Kaku T, Hayashi T, Kaneko T S. 2009. Activation of beta-glucan synthases by wall-bound purple acid phosphatase in tobacco cells. Plant Physiology, 150, 1822–1830.

Kamfwa K, Cichy K A, Kelly J D. 2015. Genome-wide association analysis of symbiotic nitrogen fixation in common bean. Theoretical and Applied Genetics, 128, 1999–2017.

Kochian L V. 2012. Plant nutrition, rooting for more phosphorus. Nature, 488, 466–467.

Li S, Chen L, Zhang L, Li X, Liu Y, Wu Z, Dong F, Wan L, Liu K, Hong D, Yang G. 2015. BnaC9, SMG7b functions as a positive regulator of the number of seeds per silique in Brassica napus by regulating the formation of functional female gametophytes. Plant Physiology, 169, 2744–2760.

Lynch J P. 2011. Root phenes for enhanced soil exploration and phosphorus acquisition, tools for future crops. Plant Physiology, 156, 1041–1049.

MacDonald G K, Bennett E M, Potter P A, Ramankutty N. 2011. Agronomic phosphorus imbalances across the world’s croplands. Proceedings of the National Academy of Sciences of the United States of America, 108, 3086–3091.

Martín A C, Pozo J C, Iglesias J, Rubio V, Solano R, Peña A, Leyva A, Paz-Ares J. 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant Journal, 24, 559–567.

Mehra P, Pandey B K, Giri J. 2017. Improvement in phosphate acquisition and utilization by a secretory purple acid phosphatase (OsPAP21b) in rice. Plant Biotechnology Journal, 15, 1054–1067.

Morcuende R, Bari R, Gibon Y, Zheng W, Pant B D, Bläsing U, Czechowski T, Udvrdi M K, Stitt M, Scheible W. 2007. Genome-wide reprogramming of metabolism and regulatory networks of Arabidopsis in response to phosphorus. Plant Cell and Environment, 30, 85–112.

Mori A, Fukuda T, Vejchasarn P, Nestler J, Pariasca-Tanaka J, Wissuwa M. 2016. The role of root size versus root efficiency in phosphorus acquisition in rice. Journal of Experimental Botany, 67, 1179–1189.

Moussa A A, Mandozai A, Qu J, Jin Y, Zhang Q, Abd El-Rahim M G, Wang P. 2021. Mapping QTLs using high-density snps genotyped by sequencing reveals novel potential regions underlying maize root morphological traits at seedling stage. International Journal of Agriculture and Biology, 25, 904–914.

Secco D, Wang C, Arpat B A, Wang Z, Poirier Y, Tyerman S D, Wu P, Shou H, Whelan J. 2012. The emerging importance of the SPX domain-containing proteins in phosphate homeostasis. New Phytologist, 193, 842–851.

Shane M W, Dixon K W, Lambers H. 2010. The occurrence of dauciform roots amongst western australian reeds, rushes and sedges, and the impact of phosphorus supply on dauciform-root development in Schoenus unispiculatus (Cyperaceae). New Phytologist, 165, 887–898.

Shi L, Shi T, Broadley M R, White P J, Long Y, Meng J, Xu F, Hammond J P. 2013. High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Annals of Botany, 112, 381–389.

Sundus Z, Tang M, Liu S, Tan X. 2022a. Candidate genes association study to identify allele-specific SNP marker of ω-3 fatty acid in Brassica napus. Journal of Plant Physiology, 248, 153–159.

Sundus Z, Tang M, Wang Y, Sarwar R, Liu S, Tan X. 2020b. Candidate genes-association study to identify loci related to oleic acid in Brassica napus using SNP markers and their heterologous expression in yeast. Plant Physiology and Biochemistry, 16, 294–302.

Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T. 2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genetics, 39, 792–796.

Takahashi Y, Teshima K M, Yokoi S, Lnnan H, Shimamoto K. 2009. Variations in hd1 proteins, hd3a promoters, and ehd1 expression levels contribute to diversity of flowering time in cultivated rice. Proceedings of the National Academy of Sciences of the United States of America, 106, 4555–4560.

Tan Z, Xie Z, Dai L, Zhang Y, Zhao H, Tang S, Hong D. 2022. Genome-and transcriptome-wide association studies reveal the genetic basis and the breeding history of seed glucosinolate content in Brassica napus. Plant Biotechnology Journal, 20, 211–225.

Wang L, Li Z, Qian W, Guo W, Gao X, Huang L, Wang H, Zhu H, Wu J W, Wang D, Liu D. 2011. The Arabidopsis purple acid phosphatase AtPAP10 is predominantly associated with the root surface and plays an important role in plant tolerance to phosphate limitation. Plant Physiology, 157, 1283–1299.

Wang X, Chen Y, Thomas C L, Ding G, Xu P, Shi D, Grandke F, Jin K, Cai H, Xu F, Yi B, Broadley M R, Shi L. 2017a. Genetic variants associated with the root system architecture of oilseed rape (Brassica napus L.) under contrasting phosphate supply. DNA Research, 24, 407–417.

Wang X, Long Y, Wang N, Zou J, Ding G, Broadley M R, White P J, Yuan P, Zhang Q, Luo Z, Liu P, Zhao H, Zhang Y, Cai H, King G J, Xu F, Meng J, Shi L. 2017b. Breeding histories and selection criteria for oilseed rape in Europe and China identified by genome wide pedigree dissection. Scientific Reports, 7, 1–11.

Wei L, Jian H, Lu K, Filardo F, Yin N, Liu L, Qu C, Li W, Du H, Li J. 2015. Genome-wide association analysis and differential expression analysis of resistance to Sclerotinia stem rot in Brassica napus. Plant Biotechnology Journal, 14, 1368–1380.

Wissuwa M. 2005. Combining a modelling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake. Plant and Soil, 269, 57–68.

Wissuwa M, Wegner J, Ae N, Yano M. 2002. Substitution mapping of Pup1, a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theoretical and Applied Genetics, 105, 890–897.

Wu W, Lin Y, Liu P, Chen Q, Tian J, Liang C. 2018. Association of extracellular dNTP utilization with a GmPAP1-like protein identified in cell wall proteomic analysis of soybean roots. Journal of Experimental Botany, 69, 603–617.

Wykoff D D, Grossman A R, Weeks D P, Usuda H, Shimogawara K. 1999. Psr1, a nuclear localized protein that regulates phosphorus metabolism in Chlamydomonas. Proceedings of the National Academy of Sciences of the United States of America, 96, 15336–15341.

Xu P, Wang X, Li H, Dai S, Cao X, Liu Z. 2022. Genetic control of the root system traits in oilseed rape under contrasting phosphate supply conditions by genome-wide association study. Plant Molecular Biology Reporter, 1, 1–13.

Yan X, Liao H, Beebe S E, Blair M W, Lynch J P. 2004. QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant and Soil, 265, 17–29.

Yang H, Liu J, Huang S, Guo T, Deng L, Hua W. 2014. Selection and evaluation of novel reference genes for quantitative reverse transcription PCR (qRT-PCR) based on genome and transcriptome data in Brassica napus L. Gene, 538, 113–122.

Yang M, Ding G, Shi L, Feng J, Xu F, Meng J. 2010. Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. Theoretical and Applied Genetics, 121, 181–193.

Zangani E, Afsahi K, Shekari F, Mac Sweeney E, Mastinu A. 2021. Nitrogen and phosphorus addition to soil improves seed yield, foliar stomatal conductance, and the photosynthetic response of rapeseed (Brassica napus L.). Agriculture, 11, 483.

Zhang D, Song H, Cheng H, Hao D, Wang H, Kan G, Jin H, Yu D. 2014. The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genetics, 10, e1004061.

Zhang Y, Thomas C L, Xiang J, Long Y, Wang X, Zou J, Luo Z, Ding G, Cai H, Graham N S, Hammond J P, King G J, White P J, Xu F, Broadley M R, Shi L, Meng J. 2016. QTL meta-analysis of root traits in Brassica napus under contrasting phosphorus supply in two growth systems. Scientific Reports, 6, 33113.

Zhang Z, Li Z, He F, Lv J, Xie B, Yi X, Li J, Li J, Song J, Pu Z, Ma J, Peng Y, Chen G, Wei Y, Zheng Y, Li W. 2023. Genome-wide association and linkage mapping strategies reveal genetic loci and candidate genes of important agronomic traits in Sichuan wheat. Journal of Integrative Agriculture, 22, 3380–3393.

No related articles found!
No Suggested Reading articles found!