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Grafting improves drought stress memory by increasing the P5CS1 gene expression in Brassica rapa

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Abstract

Aims

Plants accumulate proline as a drought-tolerance strategy. However, the effect of grafting on adaptive proline accumulation remains to be discovered.

Methods

Physiological methods were used to compare drought tolerance of turnip (B. rapa subsp. rapa) and rapeseed (B. rapa subsp. oleifera). Chromatin Immunoprecipitation (ChIP) and gene expression analysis were used to reveal epigenetic modifications and transcriptional regulation of the Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1) gene within grafting experiments.

Results

Turnip is more drought tolerant than rapeseed, accompanied by higher expression of P5CS1 gene and more proline accumulation in turnip than in rapeseed. Grafting rapeseed onto turnip improved its drought tolerance. Repeated drought stress induced stress memory in proline accumulation and markedly enhanced P5CS1–2 expression in the rapeseed scion of rapeseed/turnip (scion/rootstock) plants compared to self-grafted rapeseed plants. This accumulation required renewed histone H3K4me3 modification at the P5CS1–2 chromatin.

Conclusions

Grafting rapeseed onto turnip enhanced drought resistance in Brassica rapa through potential signaling between turnip rootstock and rapeseed scion altering epigenetic modification on the P5CS1–2 locus and increasing its transcript level during the stress memory response.

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References

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    Article  CAS  Google Scholar 

  • Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55(4):611–622

    Article  CAS  Google Scholar 

  • Cheng F, Sun R, Hou X, Zheng H, Zhang F, Zhang Y, Liu B, Liang J, Zhuang M, Liu Y, Liu D, Wang X, Li P, Liu Y, Lin K, Bucher J, Zhang N, Wang Y, Wang H, Deng J, Liao Y, Wei K, Zhang X, Fu L, Hu Y, Liu J, Cai C, Zhang S, Zhang S, Li F, Zhang H, Zhang J, Guo N, Liu Z, Liu J, Sun C, Ma Y, Zhang H, Cui Y, Freeling MR, Borm T, Bonnema G, Wu J, Wang X (2016) Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat Genet 48(10):1218–1224

    Article  CAS  Google Scholar 

  • Delauney AJ, Verma DPS (1993) Proline biosynthesis and osmoregulation in plants. Plant J 4(4):215–223

    Article  CAS  Google Scholar 

  • Ding Y, Fromm M, Avramova Z (2012) Multiple exposures to drought 'train' transcriptional responses in Arabidopsis. Nat Commun 3:740

    Article  CAS  Google Scholar 

  • Feng XJ, Li JR, Qi SL, Lin QF, Jin JB, Hua XJ (2016) Light affects salt stress-induced transcriptional memory of P5CS1 in Arabidopsis. Proc Natl Acad Sci U S A 113(51):8335–8343

    Article  CAS  Google Scholar 

  • Goldschmidt EE (2014) Plant grafting: new mechanisms, evolutionary implications. Front Plant Sci 5:727

    Article  Google Scholar 

  • Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58(13):3591–3607

    Article  CAS  Google Scholar 

  • Kesari R, Lasky JR, Villamor JG, Des Marais DL, Chen YJ, Liu TW, Lin W, Juenger TE, Verslues PE (2012) Intron-mediated alternative splicing of Arabidopsis P5CS1 and its association with natural variation in proline and climate adaptation. Proc Natl Acad Sci U S A 109(23):9197–9202

    Article  Google Scholar 

  • Liu J, Li J, Su X, Xia Z (2014) Grafting improves drought tolerance by regulating antioxidant enzyme activities and stress-responsive gene expression in tobacco. Environ Exp Bot 107:173–179

    Article  CAS  Google Scholar 

  • Melnyk CW, Meyerowitz EM (2015) Plant grafting. Curr Biol 25(5):183–188

    Article  CAS  Google Scholar 

  • Nanjo T, Fujita M, Seki M, Kato T, Tabata S, Shinozaki K (2003) Toxicity of free proline revealed in an arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell Physiol 44(5):541–548

    Article  CAS  Google Scholar 

  • Nawaz MA, Chen C, Shireen F, Zheng Z, Jiao Y, Sohail H, Afzal M, Imtiaz M, Ali MA, Yuan H (2018) Improving vanadium stress tolerance of watermelon by grafting onto bottle gourd and pumpkin rootstock. Plant Growth Regul 85(1):41–56

    Article  CAS  Google Scholar 

  • Pagliarani C, Vitali M, Ferrero M, Vitulo N, Incarbone M, Lovisolo C, Valle G, Schubert A (2017) The accumulation of miRNAs differentially modulated by drought stress is affected by grafting in grapevine. Plant Physiol 173(4):2180–2195

    Article  CAS  Google Scholar 

  • Qi X, An H, Ragsdale AP, Hall TE, Gutenkunst RN, Chris Pires J, Barker MS (2017) Genomic inferences of domestication events are corroborated by written records in Brassica rapa. Mol Ecol 26(13):3373–3388

    Article  CAS  Google Scholar 

  • Ren Y, Miao M, Meng Y, Cao J, Fan T, Yue J, Xiao F, Liu Y, Cao S (2018) DFR1-mediated inhibition of proline degradation pathway regulates drought and freezing tolerance in Arabidopsis. Cell Rep 23(13):3960–3974

    Article  CAS  Google Scholar 

  • Rouphael Y, Kyriacou MC, Colla G (2017) Vegetable grafting: a toolbox for securing yield stability under multiple stress conditions. Front Plant Sci 8:2255

    Article  Google Scholar 

  • Sailaja BS, Cohen-Carmon D, Zimmerman G, Soreq H, Meshorer E (2012) Stress-induced epigenetic transcriptional memory of acetylcholinesterase by HDAC4. Proc Natl Acad Sci U S A 109(52):3687–3695

    Article  Google Scholar 

  • Saleh A, Alvarez-Venegas R, Avramova Z (2008) An efficient chromatin immunoprecipitation (ChIP) protocol for studying histone modifications in Arabidopsis plants. Nat Protoc 3(6):1018–1025

    Article  CAS  Google Scholar 

  • Sani E, Herzyk P, Perrella G, Colot V, Amtmann A (2013) Hyperosmotic priming of Arabidopsis seedlings establishes a long-term somatic memory accompanied by specific changes of the epigenome. Genome Biol 14(6):R59

    Article  CAS  Google Scholar 

  • Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat Protoc 1(4):2019–2025

    Article  CAS  Google Scholar 

  • Szabados LL, Savourcb A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15(2):89–97

    Article  CAS  Google Scholar 

  • Székely G, Abrahám E, Cséplo A, Rigó G, Zsigmond L, Csiszár J, Ayaydin F, Strizhov N, Jásik J, Schmelzer E, Koncz C, Szabados L (2008) Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. Plant J 53(1):11–28

    Article  CAS  Google Scholar 

  • Takahashi F, Shinozaki K (2019) Long-distance signaling in plant stress response. Curr Opin Plant Biol 47:106–111

    Article  CAS  Google Scholar 

  • Turnbull CG, Booker JP, Leyser HM (2002) Micrografting techniques for testing long-distance signalling in Arabidopsis. Plant J 32(2):255–262

    Article  CAS  Google Scholar 

  • Vitale A, Rocco M, Arena S, Giuffrida F, Cassaniti C, Scaloni A, Lomaglio T, Guarnaccia V, Polizzi G, Marra M, Leonardi C (2014) Tomato susceptibility to Fusarium crown and root rot: effect of grafting combination and proteomic analysis of tolerance expression in the rootstock. Plant Physiol Biochem 83:207–216

    Article  CAS  Google Scholar 

  • Wang X, Wang H, Wang J et al (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43(10):1035–1039

    Article  CAS  Google Scholar 

  • Wang CP, Lin B, Zhang YQ, Lin YH, Liu AH, Hua XJ (2015) The evolutionary fate of Δ1-pyrroline-5-carboxylate synthetase 1 (P5CS1) genes in allotetraploid Brassica napus. J Syst Evol 52(5):566–579

    Article  Google Scholar 

  • Xin J, Dai H, Huang B (2017) Assessing the roles of roots and shoots in the accumulation of cadmium in two sweet potato cultivars using split-root and reciprocal grafting systems. Plant Soil 412(1–2):413–424

    Article  CAS  Google Scholar 

  • Yoo SD, Cho YH, Sheen J (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2(7):1565–1572

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31500221), the Natural Science Foundation of Yunnan Province (No. 2019FB056), the Major Program of National Natural Science Foundation of China (No. 31590823) and the 13th Five-year Informatization Plan of Chinese Academy of Sciences (No. XXH13506).

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Correspondence to Xiangxiang Kong or Yongping Yang.

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Luo, L., Zheng, Y., Gao, Z. et al. Grafting improves drought stress memory by increasing the P5CS1 gene expression in Brassica rapa. Plant Soil 452, 61–72 (2020). https://doi.org/10.1007/s11104-020-04547-8

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  • DOI: https://doi.org/10.1007/s11104-020-04547-8

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