You're using an outdated browser. Please upgrade to a modern browser for the best experience.
Effects of Nutrient Stress on Plant DNA Methylation: Comparison
View Latest Version
Please note this is a comparison between Version 2 by Nora Tang and Version 1 by Yong Zhang.
Nutrient limitation is major environmental stress that reduces plant growth, productivity and quality. Globally, nitrogen (N) and phosphorus (P) limitations are ubiquitous in soil. Therefore, N and P deficiencies are the main constraints of food production under low-fertilization conditions, while under high-fertilization conditions, large amounts of N and P fertilization can cause large-scale environmental pollution. In addition to N and P, breeding crops with more iron (Fe) and zinc (Zn) is also one of the priorities, since large numbers of people eat grains due to Fe and Zn deficiencies. Furthermore, there are essential nutrients for plants, such as sulfur (S), potassium (K), calcium (Ca) and magnesium (Mg). DNA methylation in plants plays a vital role in the response to nutrient changes and is involved in controlling nutrient homeostasis. 
  • DNA methylation
  • nutrient stress
  • epigenetic
  • plants
  • abiotic stress

1. Effects of Nitrogen Stress on Plant DNA Methylation

Nitrogen (N) is one of the crucial macronutrients affecting plant growth and crop yield [74][1]. When nitrogen is deficient, due to the influence of protein, nucleic acid and phospholipid synthesis in the plant, the plant will grow slowly and dwarf [75][2]. Epigenetic factors are considered to be among the essential mechanisms for plants in adapting to nitrogen deficiency [76][3]. Meyer et al. proved that RNA-dependent RNA polymerase2 (RDR2) was involved in the accumulation of biomass under N deficiency in Arabidopsis thaliana, which indicated that RdDM could be involved in the regulation of N deficiency [76][3]. Kou et al. reported that nitrogen deficiency could change DNA methylation in rice. The variation could be inherited by offspring and enhance their tolerance to nitrogen deficiency. Low nitrogen treatment induces the expression of some methylases, such as MET1, DRM1 and DRM2 [64][4]. Kuhlmann et al. reported that low nitrogen treatment in Arabidopsis thaliana affected eight shoot growth-related SNPs on chromosome 1, resulting in changes in the methylation of their recognition gene regions. They suggested that epigenetic regulation was involved in the nitrogen-use efficiency (NUE) expression of related traits. They also found RdDM-mediated asymmetric cytosine methylation changes, which affected the transcription [77][5]. Yu et al. reported that nitrogen deficiency resulted in altered methylation patterns in Leymus chinensis. They suggested that the cytosine methylation changes around transposable elements were higher than those in other genomic regions [78][6]. OurThe previous research reported that the knockdown of the high-affinity nitrate transporter partner protein OsNAR2.1 caused a decrease in nitrogen content in rice and induced DNA methylation reduction [79][7]. We also found that low nitrogen treatment causes low seed N content, which leads to DNA methylation changes in filial rice [80]. 

3.2. Effects of Phosphorus Stress on Plant DNA Methylation

2. Effects of Phosphorus Stress on Plant DNA Methylation

Phosphorus (P) is an essential macronutrient for plant growth and development [81][8]. Secco et al. reported that mC changes induced by phosphate starvation occurred preferentially in transposable elements (TEs). They suggested that, during prolonged P deprivation, TEs close to high expression stress-induced genes are hypermethylated without DCL3a, thus preventing their transcription via RNA polymerase II. Furthermore, they found that partial methylation can propagate through mitosis [82][9]. Yong-Villalobos et al. showed that phosphorus starvation leads to gene-wide methylation changes in Arabidopsis thaliana, which are accompanied by changes in gene expression. They found that phosphorus deficiency induced 20% of up-regulated differentially methylated regions (DMRs) in the shoots and 86% of up-regulated DMRs underground. They concluded that DNA methylation changes were required to regulate P sensitive genes, and DNA methylation was necessary for establishing physiological and morphological P starvation responses [83][10]. Yen et al. showed P deficiency-induced changes in the methylome. They identified over 160 DMRs between low-Pi and Pi-replete conditions. They found that the deubiquitinating enzyme OTU5 is critical for establishing DNA methylation patterns [84][11]. Tian et al. reported that phosphorus starvation caused an increase in the global methylation level, with millions of differentially methylated cytosines (DmCs) and a few hundred DMRs in tomato. They suggested that methylation changes on P might largely be shaped by TE distributions [65][12]. Schönberger et al. showed that differential methylation was associated with different P treatments with site-dependent microRNAs (miRNA). Furthermore, some miRNA sequences were directly targeted by differential methylation [85][13]. Chu et al. reported that low P induced differential methylation, and gene expression showed that the transcriptional alterations of a small part of genes were associated with methylation changes in soybean. They also found that siRNAs modulated TE activity by guiding CHH methylation in TE regions [86][14].

3.3. Effects of Other Nutrient Stresses on Plant DNA Methylation

3. Effects of Other Nutrient Stresses on Plant DNA Methylation

Zn is an essential micronutrient of all organisms in plants. Mager et al. showed that low Zn treatment could lead to massively reduced DNA methylation, and the enzymes involved in DNA maintenance methylation were repressed. They found that Zn deficiency induced a tremendous reduction in small RNA associated with DNA methylation [87][15]. Fe is an essential micronutrient in plants. Fe limitation significantly affects plant growth [88][16]. Sun et al. reported that there is widespread hypermethylation in rice after Fe deficiency, especially in the CHH context. They also found that the transcript abundance of Fe deficiency-induced genes was positive with the 24 nt siRNAs, suggesting that the alteration of methylation patterns is directed by siRNAs, which play an important role in Fe deficiency [88][16]. Bocchini et al. found that 11 DNA bands were differently methylated in Fe deficiency barleys. Furthermore, their results showed DNA methylation/demethylation patterns very similar to those of barley grown under Fe deprivation in resupplied barley, which indicated that the DNA modifications were heritable [89][17]. S is an essential element for plant organisms [73][18]. Huang et al. found that the sulfur accumulation1 (MSA1) mutant msa1 had a strong S-deficiency response compared with WT. The sulfate transporter genes SULTR1;1 and SULTR1;2 were shown to be differentially methylated in msa1 compared with WT. The results indicated that MSA1 maintained S homeostasis epigenetically via DNA methylation [73][18]. WHere summarized the effects of different nutrient stresses on plant methylation in  Table 1.
Table 1.
Summary of the effects of different nutrient stresses on plant methylation.
Element Plant Genome Region Treatment Mode of Action Methodology Reference
N Arabidopsis thaliana RDR2 −N RDR2 expression corrlated with morphological traits Quantitative real-time PCR [76][3]
N Arabidopsis thaliana AT1G55420, AT1G55430 and AT1G55440 −N DNA methylation change in recognition gene regions (AT1G55420, AT1G55430 and AT1G55440) WGBS [77][5]
N Leymus chinensis Genomic −N Cytosine methylation changes more around transposable elements AFLP, MSAP, SSAP [78][6]
N Rice Genomic −N Heritable alteration in DNA methylation MSAP [64][4]
N Rice Genomic N content decrease by the knockdown of OsNAR2.1 DNA methylation levels increase in OsNAR2.1 RNAi lines WGBS, MeDIP [79][7]
N Rice Genomic N content decrease in the parent seed Plant DNA methylation changes induced by parent seed N content WGBS [80][19]
P Rice Genomic −P DNA methylation occurred preferentially in TEs MethylC-Seq [82][9]
P Arabidopsis thaliana Genomic −P Gene-wide methylation changes WGBS [83][10]
P Arabidopsis thaliana Genomic −P Over 160 DMRs induce by P deficiency Genome-Wide DNA methylation [84][11]
P Tomato Genomic −P Global methylation level increase WGBS [65][12]
P Populus trichocarpa Genomic −P Differentially methylated miRNAs WGBS [85][13]
P Soybean Genomic −P Differential methylation, and siRNAs modulated TE activity by guiding CHH methylation BGS [86][14]
Zn Maize Genomic −Zn Major methylation loss, mostly in transposable elements BGS [87][15]
Fe Rice Genomic −Fe Hypermethylation, especially for the CHH MethylC-Seq [88][16]
Fe Barley Genomic −Fe Eleven DNA bands differently methylated the MSAP [89][17]
S Arabidopsis thaliana SULTR1.1 and SULTR1.2 −S DNA methylation of SULTR1.1 and SULTR1.2 changes in msa1 WGBS [73][18]
Note: −N: nitrogen deficiency; −P: phosphorus deficiency; −Zn: zinc deficiency; −Fe: iron deficiency; −S: sulfur deficiency; WGBS/MethylC-Seq: Whole-genome bisulfite sequencing; AFLP: Amplified fragment length polymorphism; MSAP: Methylation-sensitive amplified polymorphism; SSAP: Specific-sequence amplified polymorphism; MeDIP: Methylated DNA co-immunoprecipitation sequencing; BGS: Bisulfite genomic sequencing.

References

  1. Xu, G.; Fan, X.; Miller, A.J. Plant nitrogen assimilation and use efficiency. Annu. Rev. Plant Biol. 2012, 63, 153–182.
  2. Borrell, A.K.; Garside, A.L.; Fukai, S.; Reid, D.J. Season, nitrogen rate, and plant type affect nitrogen uptake and nitrogen use efficiency in rice. Sust. J. Agric. Res. 1998, 49, 829–843.
  3. Meyer, R.C.; Gryczka, C.; Neitsch, C.; Muller, M.; Brautigam, A.; Schlereth, A.; Schon, H.; Weigelt-Fischer, K.; Altmann, T. Genetic diversity for nitrogen use efficiency in Arabidopsis thaliana. Planta 2019, 250, 41–57.
  4. Kou, H.P.; Li, Y.; Song, X.X.; Ou, X.F.; Xing, S.C.; Ma, J.; Wettstein, D.V.; Liu, B. Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J. Plant Physiol. 2011, 168, 1685–1693.
  5. Kuhlmann, M.; Meyer, R.C.; Jia, Z.; Klose, D.; Krieg, L.-M.; von Wirén, N.; Altmann, T. Epigenetic Variation at a Genomic Locus Affecting Biomass Accumulation under Low Nitrogen in Arabidopsis thaliana. Agronomy 2020, 10, 636.
  6. Yu, Y.; Yang, X.; Wang, H.; Shi, F.; Liu, Y.; Liu, J.; Li, L.; Wang, D.; Liu, B. Cytosine methylation alteration in natural populations of Leymus chinensis induced by multiple abiotic stresses. PLoS ONE 2013, 8, e55772.
  7. Fan, X.; Chen, J.; Wu, Y.; Teo, C.; Xu, G.; Fan, X. Genetic and Global Epigenetic Modification, Which Determines the Phenotype of Transgenic Rice? Int. J. Mol. Sci. 2020, 21, 1819.
  8. López-Arredondo, D.L.; Leyva-González, M.A.; González-Morales, S.I.; López-Bucio, J.; Herrera-Estrella, L. Phosphate Nutrition: Improving Low-Phosphate Tolerance in Crops. Annu. Rev. Plant Biol. 2014, 65, 95–123.
  9. Secco, D.; Wang, C.; Shou, H.; Schultz, M.D.; Chiarenza, S.; Nussaume, L.; Ecker, J.R.; Whelan, J.; Lister, R. Stress induced gene expression drives transient DNA methylation changes at adjacent repetitive elements. eLife 2015, 4, e09343.
  10. Yong-Villalobos, L.; González-Morales, S.I.; Wrobel, K.; Gutiérrez-Alanis, D.; Cervantes-Peréz, S.A.; Hayano-Kanashiro, C.; Oropeza-Aburto, A.; Cruz-Ramírez, A.; Martínez, O.; Herrera-Estrella, L. Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc. Natl. Acad. Sci. USA 2015, 112, E7293–E7302.
  11. Yen, M.-R.; Suen, D.-F.; Hsu, F.-M.; Tsai, Y.-H.; Fu, H.; Schmidt, W.; Chen, P.-Y. Deubiquitinating Enzyme OTU5 Contributes to DNA Methylation Patterns and Is Critical for Phosphate Nutrition Signals. Plant Physiol. 2017, 175, 1826–1838.
  12. Tian, P.; Lin, Z.T.; Lin, D.B.; Dong, S.Y.; Huang, J.Z.; Huang, T.B. The pattern of DNA methylation alteration, and its association with the changes of gene expression and alternative splicing during phosphate starvation in tomato. Plant J. 2021, 108, 841–858.
  13. Schönberger, B.; Chen, X.; Mager, S.; Ludewig, U. Site-Dependent Differences in DNA Methylation and Their Impact on Plant Establishment and Phosphorus Nutrition in Populus trichocarpa. PLoS ONE 2016, 11, e0168623.
  14. Chu, S.; Zhang, X.; Yu, K.; Lv, L.; Sun, C.; Liu, X.; Zhang, J.; Jiao, Y.; Zhang, D. Genome-Wide Analysis Reveals Dynamic Epigenomic Differences in Soybean Response to Low-Phosphorus Stress. Int. J. Mol. Sci. 2020, 21, 6817.
  15. Mager, S.; Schönberger, B.; Ludewig, U. The transcriptome of zinc deficient maize roots and its relationship to DNA methylation loss. BMC Plant Biol. 2018, 18, 372.
  16. Sun, S.; Zhu, J.; Guo, R.; Whelan, J.; Shou, H. DNA methylation is involved in acclimation to iron-deficiency in rice (Oryza sativa). Plant J. 2021, 107, 727–739.
  17. Bocchini, M.; Bartucca, M.L.; Ciancaleoni, S.; Mimmo, T.; Cesco, S.; Pii, Y.; Albertini, E.; Del Buono, D. Iron deficiency in barley plants: Phytosiderophore release, iron translocation, and DNA methylation. Front. Plant Sci. 2015, 6, 514.
  18. Huang, X.; Chao, D.; Koprivova, A.; Danku, J.; Wirtz, M.; Muller, S.; Sandoval, F.J.; Bauwe, H.; Roje, S.; Dilkes, B.; et al. Nuclear localised MORE SULPHUR ACCUMULATION1 epigenetically regulates sulphur homeostasis in Arabidopsis thaliana. PLoS Genet. 2016, 12, e1006298.
  19. Fan, X.; Liu, L.; Qian, K.; Chen, J.; Zhang, Y.; Xie, P.; Xu, M.; Hu, Z.; Yan, W.; Wu, Y.; et al. Plant DNA methylation is sensitive to parent seed N content and influences the growth of rice. BMC Plant Biol. 2021, 21, 211.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/)
Academic Video Service
Feedback