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Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Identification and analysis of the gene network involved in phosphorus uptake in maize

Maryam Razmjou https://orcid.org/0009-0005-4953-1253 A , Reza Darvishzadeh https://orcid.org/0000-0001-5991-4411 A * , Hadi Alipour https://orcid.org/0000-0003-0086-002X A * , Ebrahim Sepehr https://orcid.org/0000-0001-5843-0669 B , Hamid Hatami Maleki https://orcid.org/0000-0001-7179-861X C , Sorour Arzhang https://orcid.org/0000-0002-4114-2828 A and Omid Mohammad Alizadeh D
+ Author Affiliations
- Author Affiliations

A Department of Plant Production and Genetics, Faculty of Agriculture, Urmia University, Urmia, Iran.

B Department of Soil Science, Faculty of Agriculture, Urmia University, Urmia, Iran.

C Department of Plant Production and Genetics, Faculty of Agriculture, University of Maragheh, Maragheh, Iran.

D Department of Agricultural Biotechnology, University of Tehran, Karaj, Iran.


Handling Editor: Enrico Francia

Crop & Pasture Science 76, CP25055 https://doi.org/10.1071/CP25055
Submitted: 3 March 2025  Accepted: 8 March 2025  Published: 26 March 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Phosphorus deficiency is a limiting factor affecting plant growth, development, and yield.

Aims

This study aimed to evaluate the Iranian maize (Zea mays) germplasm in response phosphorus deficiency and identify genomic loci involved in the response.

Methods

Using a maize 600K Single Nucleotide Polymorphism (SNP) array followed by gene network analysis, a genetic analysis of phosphorus uptake of 93 maize genotypes was evaluated in optimal and phosphorus-deficient conditions. After filtering for a minor allele frequency below 10%, 450,133 SNPs were retained to investigate phosphorus uptake efficiency.

Key results

In both optimal and deficient phosphorus states, seven candidate genes were identified that corresponded with disease resistance proteins (e.g. RPM1 and RPP13), cellular component proteins (e.g. RER3), molecular functional protein (e.g. SF3B4), and other proteins including HVA22-like protein c and PPR. Genes RPM1 and RPP13 interacted with RIN genes that act as essential regulators of the plant defence system. The candidate gene HVA22C could interact with other HVA22 genes to protect cells against environmental stresses.

Conclusions

The identified candidate genes play roles in the abscisic acid signalling pathway, mesophyll cell division, plant defence regulation against pathogens, and chloroplast RNA processing. This preliminary study offered valuable insights, but further validation is needed before drawing definitive conclusions.

Implications

There was genetic variability for phosphorus uptake among the Iranian maize germplasm and the identified genes could applied in future breeding programs of maize to better understand the molecular response to phosphorus deficiency in the development of more phosphorus-efficient maize genotypes.

Keywords: gene ontology, gene regulatory network, genome-wide association studies, Maize 600k SNP array, molecular breeding, molecular markers, phosphorus deficiency, post-GWAS.

References

Afzal A, Bano A (2008) Rhizobium and phosphate solubilizing bacteria improve the yield and phosphorus uptake in wheat (Triticum aestivum). International Journal of Agriculture and Biology 10, 1560-1566.
| Google Scholar |

Arab M, Kazemitabar SK, Hashemipetroudi SH (2022) Bioinformatics analysis of CBL gene family members in Sesamum indicum under drought stress. Crop Biotechnology 11, 17-31.
| Crossref | Google Scholar |

Arzhang S, Darvishzadeh R, Alipour H, Maleki HH, Dezhsetan S (2024) Genetic variability of maize (Zea mays) germplasm from Iran: genotyping with a maize 600K SNP array and genome-wide scanning for selection signatures. Crop & Pasture Science 75, CP23288.
| Crossref | Google Scholar |

Bagayoko M, Alvey S, Neumann G, Buerkert A (2000) Root-induced increases in soil pH and nutrient availability to field-grown cereals and legumes on acid sandy soils of Sudano-Sahelian West Africa. Plant and Soil 225, 117-127.
| Crossref | Google Scholar |

Baker A, Ceasar SA, Palmer AJ, Paterson JB, Qi W, Muench SP, Baldwin SA (2015) Replace, reuse, recycle: Improving the sustainable use of phosphorus by plants. Journal of Experimental Botany 66, 3523-3540.
| Crossref | Google Scholar |

Baum D (2008) Reading a phylogenetic tree: the meaning of monophyletic groups. Nature Education 1, 190.
| Google Scholar |

Breseghello F, Sorrells ME (2006) Association analysis as a strategy for improvement of quantitative traits in plants. Crop Science 46, 1323-1330.
| Crossref | Google Scholar |

Cheng J, Fan H, Li L, Hu B, Liu H, Liu Z (2018) Genome-wide identification and expression analyses of RPP13-like genes in barley. Biochip Journal 12, 102-113.
| Crossref | Google Scholar |

Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Global Environmental Change 19, 292-305.
| Crossref | Google Scholar |

Dawson CJ, Hilton J (2011) Fertiliser availability in a resource-limited world: production and recycling of nitrogen and phosphorus. Food Policy 36, S14-S22.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Falconer DS (1989) ‘Introduction to quantitative genetics.’ 3rd edn (Longman Scientific and Technical: New York, NY, USA)

Heuer S, Chin JH, Gamuyao R, Haefele SM, Wissuwa M (2013) Molecular breeding for phosphorus-efficient rice. In ‘Translational genomics for crop breeding: abiotic stress, yield and quality. Volume II: abiotic stress, yield and quality’. (Eds R Varshney, S Tuberosa) pp. 65–82. (Wiley: New York, NY, USA) 10.1002/9781118728482.ch5

Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, López-Arredondo D, Wissuwa M, Delhaize E, Rouached H (2017) Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant Journal 90, 868-885.
| Crossref | Google Scholar |

Huang M, Liu X, Zhou Y, Summers RM, Zhang Z (2019) BLINK: a package for the next level of genome-wide association studies with both individuals and markers in the millions. Gigascience 8(2), giy154.
| Crossref | Google Scholar |

Johnson HW, Robinson HF, Comstock RE (1955) Estimates of genetic and environmental variability in soybeans. Agronomy Journal 47, 314-318.
| Crossref | Google Scholar |

Kalia RK, Rai MK, Kalia S, Singh R, Dhawan AK (2011) Microsatellite markers: an overview of the recent progress in plants. Euphytica 177, 309-334.
| Crossref | Google Scholar |

Krem MM, Di Cera E (2001) Molecular markers of serine protease evolution. EMBO Journal 20, 3036-3045.
| Crossref | Google Scholar |

Kumar V, Singh TR, Hada A, Jolly M, Ganapathi A, Sachdev A (2015) Probing phosphorus efficient low phytic acid content soybean genotypes with phosphorus starvation in hydroponics growth system. Applied Biochemistry and Biotechnology 177, 689-699.
| Crossref | Google Scholar |

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.
| Crossref | Google Scholar |

Lee HK, Hsu AK, Sajdak J, Qin J, Pavlidis P (2004) Coexpression analysis of human genes across many microarray data sets. Genome Research 14, 1085-1094.
| Crossref | Google Scholar |

Li D, Wang H, Wang M, Li G, Chen Z, Leiser WL, Weiß TM, Lu X, Wang M, Chen S, Chen F, Yuan L, Würschum T, Liu W (2021) Genetic dissection of phosphorus use efficiency in a maize association population under two p levels in the field. International Journal of Molecular Sciences 22, 9311.
| Crossref | Google Scholar |

Lu Y, Yan J, Guimarães CT, Taba S, Hao Z, Gao S, Chen S, Li J, Zhang S, Vivek BS, Magorokosho C, Mugo S, Makumbi D, Parentoni SN, Shah T, Rong T, Crouch JH, Xu Y (2009) Molecular characterization of global maize breeding germplasm based on genome-wide single nucleotide polymorphisms. Theoretical and Applied Genetics 120, 93-115.
| Crossref | Google Scholar |

Luo B, Ma P, Nie Z, Zhang X, He X, Ding X, Feng X, Lu Q, Ren Z, Lin H, Wu Y, Shen Y, Zhang S, Wu L, Liu D, Pan G, Rong T, Gao S (2019) Metabolite profiling and genome-wide association studies reveal response mechanisms of phosphorus deficiency in maize seedling. Plant Journal 97, 947-969.
| Crossref | Google Scholar |

Magar BT, Acharya S, Gyawali B, Timilsena K, Upadhayaya J, Shrestha J (2021) Genetic variability and trait association in maize (Zea mays L.) varieties for growth and yield traits. Heliyon 7, e07939.
| Crossref | Google Scholar |

Maleki HH, Mohammadi R, Arshad M, Hasanzadeh M, Rafiee M (2023) Genetic variability and population structure of Agropyron desertorum accessions from Iran based on inter simple sequence repeat (ISSR) assay. Genetic Resources and Crop Evolution 70, 2511-2520.
| Crossref | Google Scholar |

Manschadi AM, Kaul HP, Vollmann J, Eitzinger J, Wenzel W (2014) Developing phosphorus-efficient crop varieties—An interdisciplinary research framework. Field Crops Research 162, 87-98.
| Crossref | Google Scholar |

Mbithi-Mwikya S, Van Camp J, Yiru Y, Huyghebaert A (2000) Nutrient and antinutrient changes in finger millet (Eleusine coracan) during sprouting. LWT 33, 9-14.
| Crossref | Google Scholar |

Mendes FF, Guimarães LJM, Souza JC, Guimarães PEO, Magalhaes JV, Garcia AAF, Parentoni SN, Guimaraes CT (2014) Genetic architecture of phosphorus use efficiency in tropical maize cultivated in a low-P soil. Crop Science 54, 1530-1538.
| Crossref | Google Scholar |

Neupane B, Poudel A, Wagle P (2020) Varietal evaluation of promising maize genotypes in mid hills of Nepal. Journal of Agriculture and Natural Resources 3, 127-139.
| Crossref | Google Scholar |

Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) ‘Estimation of available phosphorus in soils by extraction with sodium bicarbonate.’ (United States Department of Agriculture: Washington, DC, USA) pp. 1–19.

Peiffer JA, Romay MC, Gore MA, Flint-Garcia SA, Zhang Z, Millard MJ, Gardner CAC, McMullen MD, Holland JB, Bradbury PJ, Buckler ES (2014) The genetic architecture of maize height. Genetics 196, 1337-1356.
| Crossref | Google Scholar |

Pevsner J (2009) ‘Bioinformatics and functional genomics.’ 2nd edn. (John Wiley & Sons, Ltd) 10.1002/9780470451496

Qiu H, Mei X, Liu C, Wang J, Wang G, Wang X, Liu Z, Cai Y (2013) Fine mapping of quantitative trait loci for acid phosphatase activity in maize leaf under low phosphorus stress. Molecular Breeding 32, 629-639.
| Crossref | Google Scholar |

Sandaña P, Pinochet D (2014) Grain yield and phosphorus use efficiency of wheat and pea in a high yielding environment. Journal of Soil Science and Plant Nutrition 14, 973-986.
| Crossref | Google Scholar |

Shahbazi K, Besharati H (2013) Overview of agricultural soil fertility status of Iran. Land Management Journal 1, 1-15.
| Crossref | Google Scholar |

Shahrokhi M, Khorasani SK, Ebrahimi A (2013) Study of genetic components in various maize (Zea mays L.) traits, using generation mean analysis method. International Journal of Agronomy and Plant Production 4, 405-412.
| Google Scholar |

Shen Q, Uknes SJ, Ho THD (1993) Hormone response complex in a novel abscisic acid and cycloheximide-inducible barley gene. Journal of Biological Chemistry 268, 23652-23660.
| Crossref | Google Scholar |

Shen Q, Chen CN, Brands A, Pan SM, David Ho TH (2001) The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms. Plant Molecular Biology 45, 327-340.
| Crossref | Google Scholar |

Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiology 156, 997-1005.
| Crossref | Google Scholar |

Spataro G, Tiranti B, Arcaleni P, Bellucci E, Attene G, Papa R, Spagnoletti Zeuli P, Negri V (2011) Genetic diversity and structure of a worldwide collection of Phaseolus coccineus L. Theoretical and Applied Genetics 122(7), 1281-1291.
| Crossref | Google Scholar |

Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302, 249-255.
| Crossref | Google Scholar |

Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytologist 157, 423-447.
| Crossref | Google Scholar |

Vinod KK (2015) Enhancing nutrient starvation tolerance in rice. In ‘Genetic manipulation in plants for mitigation of climate change’. (Eds PK Jaiwal, RP Singh, OP Dhankher) pp. 117–142. (Springer: New Delhi, India) 10.1007/978-81-322-2662-8_6

Wang JZ, Du Z, Payattakool R, Yu PS, Chen CF (2007) A new method to measure the semantic similarity of GO terms. Bioinformatics 23, 1274-1281.
| Crossref | Google Scholar |

Wang QJ, Yuan Y, Liao Z, Jiang Y, Wang Q, Zhang L, Gao S, Wu F, Li M, Xie W, Liu T, Xu J, Liu Y, Feng X, Lu Y (2019) Genome-wide association study of 13 traits in maize seedlings under low phosphorus stress. The Plant Genome 12, 1-13.
| Crossref | Google Scholar |

Wu X, Li Y, Shi Y, Song Y, Zhang D, Li C, Buckler ES, Li Y, Zhang Z, Wang T (2016) Joint-linkage mapping and GWAS reveal extensive genetic loci that regulate male inflorescence size in maize. Plant Biotechnology Journal 14, 1551-1562.
| Crossref | Google Scholar |

Xu C, Zhang H, Sun J, Guo Z, Zou C, Li WX, Xie C, Huang C, Xu R, Liao H, Wang J, Xu X, Wang S, Xu Y (2018) Genome-wide association study dissects yield components associated with low-phosphorus stress tolerance in maize. Theoretical and Applied Genetics 131, 1699-1714.
| Crossref | Google Scholar |

Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4, e8451.
| Crossref | Google Scholar |

Zhang G, Wang X, Wang B, Tian Y, Li M, Nie Y, Peng Q, Wang Z (2013) Fine mapping a major QTL for kernel number per row under different phosphorus regimes in maize (Zea mays L.). Theoretical and Applied Genetics 126, 1545–1553. 10.1007/s00122-013-2072-2

Zhu XM, Shao XY, Pei YH, Guo XM, Li J, Song XY, Zhao MA (2018) Genetic diversity and genome-wide association study of major ear quantitative traits using high-density SNPs in maize. Frontiers in Plant Science 9, 966.
| Crossref | Google Scholar |