Abstract
Phosphorus deficiency is one of the major factors limiting plant growth and grain yield. Improving plant tolerance to Pi deficiency through genetic mechanism is an important source to increase grain yield. In this study, bioinformatics analysis, expression, and natural variation in ZmNAC134 gene with low Pi tolerant traits were analyzed under low Pi conditions. A total of 177 diverse heterotic groups of maize inbreds were used to identify the nucleotide diversity and alleles of ZmNAC134, which plays a vital role in the regulation of root architecture in response to Pi deficiency evolutionary results showed that ZmNAC134 has 3 homologous genes and these genes have one exon and conserved domain. The phenotypic traits showed significant difference for each of the 22 traits under deficient and sufficient Pi conditions. A total of 27 SNPs were identified in the coding region of ZmNAC134 and no InDels among 177 inbred lines. Among 27 SNPs, a total of 8 sites were highly significantly associated with multiple traits of low Pi tolerant trait index at − log10 P = 3.43. Although, 7 sites under Pi normal and 9 sites under Pi deficient conditions, of which four synonymous sites (position S24, S82, S164, and S1037) were associated with diverse number of traits in low Pi and normal Pi conditions and LD was not tight among these sites. Furthermore, the expression pattern was compared between Pi tolerant 178 and Pi sensitive 9782 inbred lines. ZmNAC134 was highly up-regulated in the roots and leaves of Pi tolerant 178 inbred line at 3 days, 7 days, and 9 days in roots and 7 days and 12 days in leaves while down-regulated in roots and leaves of Pi sensitive 9782 inbred line. In addition, protein encoded by ZmNAC134 was located in both nucleus and cytoplasm. Our findings provide the new insight of ZmNAC134 gene involved in low Pi stress and responsible against low Pi condition and the significant association of polymorphic loci with traits could be helpful to find out the molecular marker for genetic resources for further molecular maize breeding program.
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References
Bradbury P, Zhang Z, Kroon D, Casstevens TY, Buckler E (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635
Brownawell AM, Kops GJ, Macara IG, Burgering BM (2001) Inhibition of nuclear import by protein kinase B (Akt) regulates the subcellular distribution and activity of the fork head transcription factor AFX. Mol Cell Biol 21:3534–3546
Cai H, Xie W, Zhu T, Lian X (2012) Transcriptome response to phosphorus starvation in rice. Acta Physiol Plant 34(1):327–341
Calderonvazquez C, Ibarralaclette E, Caballeroperez J, Herreraestrella L (2008) Transcript profiling of Zea mays roots reveals gene responses to phosphate deficiency at the plant- and species-specific levels. J Exp Bot 59(9):2479–2497
Ching A, Caldwell KS, Jung M, Dolan M, Smith OS, Tingey S, Morgante M, Rafalski AJ (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3(1):19
Chin-Sheng Y, Chih-Wen C, Wen-Chi S, Kuei-Chung C, Shao-Wei H, Jenn-Kang H, Chih-Hao L (2014) CELLO2GO: a web server for protein subCELlular LOcalization prediction with functional gene ontology annotation. PLoS ONE 9(6):e99368
Clark RM, Eric L, Joachim M, Doebley JF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci USA 101(3):700–707
Dan Z, Haina S, Hao C, Derong H, Hui W, Guizhen K, Hangxia J, Deyue Y (2014) The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 10(1):e1004061
Fang Y, Liao K, Du H, Xu Y, Song H, Li X, Xiong L (2015) A stress-responsive NAC transcription factor SNAC3 confers heat and drought tolerance through modulation of reactive oxygen species in rice. J Exp Bot 66(21):6803–6817
Font i Forcada C, Guajardo V, Reyes Chin Wo S, Moreno Sánchez MÁ (2018) Association mapping analysis for fruit quality traits in Prunus persica using SNP markers. Front Plant Sci 9:2005
Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, Mcmullen MD, Grills GS, Rossibarra J (2009) A first-generation haplotype map of maize. Science 326(5956):1115–1117
Guo A, Zhu Q, Chen X, Luo J (2007) GSDS: a gene structure display server. Yi Chuan Hereditas 29(8):1023–1026
Hyeon-Son C, Wen-Min S, Gil-Soo H, Devin P, Zhi X, Carman GM (2012) Pho85p–Pho80p phosphorylation of yeast Pah1p phosphatidate phosphatase regulates its activity, location, abundance, and function in lipid metabolism. J Biol Chem 287(14):11290–11301
Jensen MK, Kjaersgaard T, Nielsen MM, Galberg P, Petersen K, O’Shea C, Skriver K (2010) The Arabidopsis thaliana NAC transcription factor family: structure-function relationships and determinants of ANAC019 stress signalling. Biochem J 426(7):183–196
Kai F, Ming W, Ying M, Mi N, Noreen B, Shuna Y, Feng L, Xuede W (2014) Molecular evolution and expansion analysis of the NAC transcription factor in Zea mays. PLoS ONE 9(11):e111837
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874
Kumiko O, Akifumi S, Yutaka O, Toru F, Toru M (2011) Suppression of a NAC-like transcription factor gene improves boron-toxicity tolerance in rice. Plant Physiol 156(3):1457–1463
Li Z, Gao Q, Liu Y, He C, Zhang X, Zhang J (2011) Overexpression of transcription factor ZmPTF1 improves low phosphate tolerance of maize by regulating carbon metabolism and root growth. Planta 233:1129–1143
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lin H-J, Gao J, Zhang Z-M, Shen Y-O, Lan H, Liu L, Xiang K, Zhao M, Zhou S, Zhang Y-Z (2013) Transcriptional responses of maize seedling root to phosphorus starvation. Mol Biol Rep 40(9):5359–5379
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2(−delta delta c(t)) method. Methods 25(4):402–408
Lopezarredondo DL, Leyvagonzalez MA, Gonzalezmorales SI, Lopezbucio J, Herreraestrella LR (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65(1):95–123
Lu Y, Zhang S, Shah T, Xie C, Hao Z, Li X, Farkhari M, Ribaut JM, Cao M, Rong T (2010) Joint linkage–linkage disequilibrium mapping is a powerful approach to detecting quantitative trait loci underlying drought tolerance in maize. Proc Natl Acad Sci 107(45):19585–19590
Luo B, Ma P, Nie Z, Zhang X, He X, Ding X, Feng X, Lu Q, Ren Z, Lin H (2019) Metabolite profiling and genome-wide association studies reveal response mechanisms of phosphorus deficiency in maize seedling. Plant J 97:947–969
Mao H, Wang H, Liu S, Li Z, Yang X, Yan J, Li J, Tran LP, Qin F (2015) A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nat Commun 6(1):8326
Nilsson L, Muller R, Nielsen TH (2010) Dissecting the plant transcriptome and the regulatory responses to phosphate deprivation. Physiol Plant 139(2):129–143
Nuruzzaman M, Manimekalai R, Sharoni AM, Satoh K, Kondoh H, Ooka H, Kikuchi S (2010) Genome-wide analysis of NAC transcription factor family in rice. Gene 465(1):30–44
Nuruzzaman M, Sharoni AM, Kikuchi S (2013) Roles of NAC transcription factors in the regulation of biotic and abiotic stress responses in plants. Front Microbiol 4(4):248
Olsen AN, Ernst HA, Leggio LL, Skriver K (2005) NAC transcription factors: structurally distinct, functionally diverse. Trends Plant Sci 10(2):79–87
Ooka H, Satoh K, Doi K, Nagata T, Otomo Y, Murakami K, Matsubara K, Osato N, Kawai J, Carninci P (2003) Comprehensive analysis of NAC family genes in Oryza sativa and Arabidopsis thaliana. DNA Res 10(6):239–247
Parnell E, Smith BO, Yarwood SJ (2015) The cAMP sensors, EPAC1 and EPAC2, display distinct subcellular distributions despite sharing a common nuclear pore localisation signal. Cell Signal 27(5):989–996
Peng X, Zhao Y, Li X, Wu M, Chai W, Sheng L, Wang Y, Dong Q, Jiang H, Cheng B (2015) Genomewide identification, classification and analysis of NAC type gene family in maize. J Genet 94(3):377–390
Peret B, Clement M, Nussaume L, Desnos T (2011) Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci 16(8):442–450
Ping W, Huixia S, Guohua X, Xinming L (2013) Improvement of phosphorus efficiency in rice on the basis of understanding phosphate signaling and homeostasis. Curr Opin Plant Biol 16(2):205–212
Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15(1):8–15
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Puranik S, Sahu PP, Srivastava PS, Prasad M (2012) NAC proteins: regulation and role in stress tolerance. Trends Plant Sci 17(6):369–381
Puranik S, Sahu PP, Mandal SN, Suresh BV, Parida SK, Prasad M (2013) Comprehensive genome-wide survey, genomic constitution and expression profiling of the NAC transcription factor family in foxtail millet (Setaria italica L.). Plos ONE 8(5):e64594
Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98(20):11479–11484
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F (2011) Phosphorus dynamics: from soil to plant. Plant Physiol 156(3):997–1005
Shengxue L, Xianglan W, Hongwei W, Haibo X, Xiaohong Y, Jianbing Y, Jiansheng L, Lam-Son Phan T, Kazuo S, Kazuko YS (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9(9):e1003790
Shun-zhong L, Yan-li H, Zhang S, Shen Y, Zhang H (2014) Genome-wide expression profile of maize root response to phosphorus deficiency revealed by deep sequencing. J Integr Agric 13(6):1216–1229
Strable J, Scanlon MJ (2009) Maize (Zea mays): a model organism for basic and applied research in plant biology. Cold Spring Harb Protoc 2009(10):pdb.emo132
Su Z, Li X, Hao Z, Xie C, Li M, Weng J, Zhang D, Liang X, Wang Z, Gao J (2011) Association analysis of the nced and rab28 genes with phenotypic traits under water stress in maize. Plant Mol Biol Rep 29(3):714–722
Sun Y, Mu C, Chen Y, Kong X, Xu Y, Zheng H, Zhang H, Wang Q, Xue Y, Li Z (2016) Comparative transcript profiling of maize inbreds in response to long-term phosphorus deficiency stress. Plant Physiol Biochem 109:467–481
Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS (2001) Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA 98(16):9161–9166
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform Chapter 2 (Unit 2):Unit 2.3
Thornton B, Basu C (2015) Rapid and simple method of qPCR primer design. Methods Mol Biol 1275:173–179
Tian F, Stevens NM, Buckler ES (2009) Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10. Proc Natl Acad Sci USA 106(24):9979–9986
Wang X, Wang H, Liu S, Ferjani A, Li J, Yan J, Yang X, Qin F (2016) Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nat Genet 48(10):1233
Weng J, Li B, Liu C, Yang X, Wang H, Hao Z, Li M, Zhang D, Ci X, Li X (2013) A non-synonymous SNP within the isopentenyl transferase 2 locus is associated with kernel weight in Chinese maize inbreds (Zea mays L.). BMC Plant Biol 13(1):98
Wilson LM, Whitt SR, Ibáñez AM, Rocheford TR, Goodman MM, Buckler ES (2004) Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16(10):2719–2733
Wu X, Yang H, Qu C, Xu Z, Li W, Hao B, Yang C, Sun G, Liu G (2015) Sequence and expression analysis of the AMT gene family in poplar. Front Plant Sci 6:337
Wu F, Liu Z, Xu J, Gao S, Lin H, Liu L, Liu Y, Lu Y (2016) Molecular evolution and association of natural variation in ZmARF31 with low phosphorus tolerance in maize. Front Plant Sci 7:1076
Xiang Y, Sun X, Gao S, Qin F, Dai M (2017) Deletion of an endoplasmic reticulum stress response element in a ZmPP2C-A gene facilitates drought tolerance of maize seedlings. Mol Plant 10(3):456–469
Yan J, Warburton ML, Crouch JH (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51(2):433–449
Yang Q, Li Z, Li W, Ku L, Wang C, Ye J, Li K, Yang N, Li Y, Zhong T (2013) CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proc Natl Acad Sci 110(42):16969–16974
Yang N, Lu Y, Yang X, Huang J, Zhou Y, Ali F, Wen W, Liu J, Li J, Yan J (2014a) Genome wide association studies using a new nonparametric model reveal the genetic architecture of 17 agronomic traits in an enlarged maize association panel. PLOS Genet 10(9):e1004573
Yang Z, Zhang E, Jiang Y, Xu S, Liang P, Chen Q, Xu C (2014b) Sequence polymorphisms in Zmisa2 gene are significantly associated with starch pasting and gelatinization properties in maize (Zea mays L.). Mol Breed 34(4):1833–1842
Yu J, Buckler ES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotechnol 17(2):155–160
Yu X, Bai G, Liu S, Luo N, Wang Y, Richmond DS, Pijut PM, Jackson SA, Yu J, Jiang Y (2013) Association of candidate genes with drought tolerance traits in diverse perennial ryegrass accessions. J Exp Bot 64(6):1537–1551
Zhang X, Zhang H, Li L, Lan H, Ren Z, Liu D, Wu L, Liu H, Jaqueth J, Li B (2016) Characterizing the population structure and genetic diversity of maize breeding germplasm in Southwest China using genome-wide SNP markers. BMC Genom 17(1):697
Zhang Y, Wan J, He L, Lan H, Li L (2019) Genome-wide association analysis of plant height using the maize F1 population. Plants 8(10):432
Zhu T, Budworth P, Han B, Brown D, Chang HS, Zou G, Wang X (2001) Toward elucidating the global gene expression patterns of developing Arabidopsis: parallel analysis of 8300 genes by a high-density oligonucleotide probe array. Plant Physiol Biochem 39(3):221–242
Acknowledgements
This research was funded by a grants from the Sichuan Science and Technology Support Project (2016NZ0103, 2016NYZ0043, and 2018HH0013.), Sichuan Financial Innovation Capacity Improvement Project Special Fund (2016NYPZ-104), China Agricultural Research System (CARS-02), and National Natural Foundation of China (31971955).
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JHS and SG designed the experiment, writing original draft and approved for final draft; JHS, LB, and XH conducted the experiments; JHS, FZ, HT, XZ, DL, LW, XD, and PM analyzed the data, prepared the tables and figures and approved the final draft; Shibin Gao supervision and approved final draft.
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Sahito, J.H., Zheng, F., Tang, H. et al. Identification, association, and expression analysis of ZmNAC134 gene response to phosphorus deficiency tolerance traits in maize at seedling stage. Euphytica 216, 100 (2020). https://doi.org/10.1007/s10681-020-02634-6
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DOI: https://doi.org/10.1007/s10681-020-02634-6