Heterogeneous root zone salinity mitigates salt injury to Sorghum bicolor (L.) Moench in a split-root system

Autoři: Huawen Zhang aff001;  Runfeng Wang aff002;  Hailian Wang aff002;  Bin Liu aff002;  Mengping Xu aff002;  Yan’an Guan aff002;  Yanbing Yang aff002;  Ling Qin aff002;  Erying Chen aff002;  Feifei Li aff002;  Ruidong Huang aff001;  Yufei Zhou aff001
Působiště autorů: Agronomy College, Shenyang Agricultural University, Shenyang, Liaoning, China aff001;  Crop Research Institute, Shandong Academy of Agricultural Sciences, Jinan, Shandong, China aff002;  Shandong Engineering Laboratory for Featured Crops, Jinan, Shandong, China aff003
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227020


The heterogeneous distribution of soil salinity across the rhizosphere can moderate salt injury and improve sorghum growth. However, the essential molecular mechanisms used by sorghum to adapt to such environmental conditions remain uncharacterized. The present study evaluated physiological parameters such as the photosynthetic rate, antioxidative enzyme activities, leaf Na+ and K+ contents, and osmolyte contents and investigated gene expression patterns via RNA sequencing (RNA-seq) analysis under various conditions of nonuniformly distributed salt. Totals of 5691 and 2047 differentially expressed genes (DEGs) in the leaves and roots, respectively, were identified by RNA-seq under nonuniform (NaCl-free and 200 mmol·L-1 NaCl) and uniform (100 mmol·L-1 and 100 mmol·L-1 NaCl) salinity conditions. The expression of genes related to photosynthesis, Na+ compartmentalization, phytohormone metabolism, antioxidative enzymes, and transcription factors (TFs) was enhanced in leaves under nonuniform salinity stress compared with uniform salinity stress. Similarly, the expression of the majority of aquaporins and essential mineral transporters was upregulated in the NaCl-free root side in the nonuniform salinity treatment, whereas abscisic acid (ABA)-related and salt stress-responsive TF transcripts were more abundant in the high-saline root side in the nonuniform salinity treatment. In contrast, the expression of the DEGs identified in the nonuniform salinity treatment remained virtually unaffected and was even downregulated in the uniform salinity treatment. The transcriptome findings might be supportive of the increased photosynthetic rate, reduced Na+ levels, increased antioxidative capability in the leaves and, consequently, the growth recovery of sorghum under nonuniform salinity stress as well as the inhibited sorghum growth under uniform salinity conditions. The increased expression of salt resistance genes activated in response to the nonuniform salinity distribution implied that the cross-talk between the nonsaline and high-saline sides of the roots exposed to nonuniform salt stress is potentially regulated.

Klíčová slova:

Arabidopsis thaliana – DNA transcription – Gene expression – Leaves – Oryza – Plant resistance to abiotic stress – Salinity – Transcription factors


1. Le Gall H, Philippe F, Domon JM, Gillet F, Pelloux J, Rayon C. Cell wall metabolism in response to abiotic stress. Plants-Basel. 2015; 4(1), 112–166. doi: 10.3390/plants4010112 27135320

2. Zhang H, Han B, Wang T, Chen SX, Li HY, Zhang YH, et al. Mechanisms of plant salt response: Insights from proteomics. Journal of Proteome Research. 2012; 11(1), 49–67. doi: 10.1021/pr200861w 22017755

3. Singh M, Singh A, Prasad SM, Singh RK. Regulation of plants metabolism in response to salt stress: An omics approach. Acta Physiologiae Plantarum. 2017; 39, 48–65. doi: 10.1007/s11738-016-2345-x

4. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry. 2010; 48, 909–930. doi: 10.1016/j.plaphy.2010.08.016 20870416

5. James RA, Blake C, Byrt CS, Munns R. Major genes for Na+ exclusion, Nax1 and Nax2 (wheat HKT1;4 and HKT1;5), decrease Na+ accumulation in bread wheat leaves under saline and waterlogged conditions. Journal of Experimental Botany. 2011; 62(8), 2939–2947. doi: 10.1093/jxb/err003 21357768

6. Kong XQ, Luo Z, Dong HZ, Li WJ, Chen YZ. Non-uniform salinity in the root zone alleviates salt damage by increasing sodium, water and nutrient transport genes expression in cotton. Scientific Reports. 2017; 7(1), 2879–2892. doi: 10.1038/s41598-017-03302-x 28588258

7. Wu SJ, Ding L, Zhu JK. SOS1, a genetic locus essential for salt tolerance and potassium acquisition. Plant Cell. 1996; 8(4), 617–627. doi: 10.1105/tpc.8.4.617 12239394

8. Liu J, Zhu J. Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiology. 1997; 114(2), 591–596. doi: 10.1104/pp.114.2.591 9193091

9. Zhu JK, Liu JP, Xiong LM. Genetic analysis of salt tolerance in Arabidopsis: Evidence for a critical role of potassium nutrition. Plant Cell. 1998; 10(7), 1181–1191. doi: 10.1105/tpc.10.7.1181 9668136

10. Munns R, Rebetzke GJ, Husain S, James RA, Hare RA. Genetic control of sodium exclusion in durum wheat. Australian Journal of Agricultural Research. 2003; 54(7), 627–635. doi: 10.1071/AR03027

11. Tester M, Davenport R. Na+ tolerance and Na+ transport in higher plants. Annals of Botany. 2003; 91(5), 503–527. doi: 10.1093/aob/mcg058 12646496

12. Afzal Z, Howton T, Sun Y, Mukhtar M. The roles of aquaporins in plant stress responses. Journal of Developmental Biology. 2016; 4(1), 9–31. doi: 10.3390/jdb4010009 29615577

13. Ryu HJ, Cho YG. Plant hormones in salt stress tolerance. Journal of Plant Biology. 2015; 58(3), 147–155. doi: 10.1007/s12374-015-0103-z

14. Hu YR, Jiang YJ, Han X, Wang HP, Pan JJ, Yu DQ. Jasmonate regulates leaf senescence and tolerance to cold stress: Crosstalk with other phytohormones. Journal of Experimental Botany. 2017; 68(6), 1361–1369. doi: 10.1093/jxb/erx004 28201612

15. Borsani O, Valpuesta V, Botella MA. Evidence for a role of salicylic acid in the oxidative damage generated by NaCl and osmotic stress in Arabidopsis seedlings. Plant Physiology. 2001; 126, 1024–1030. doi: 10.1104/pp.126.3.1024 11457953

16. Bazihizina N, Barrett-Lennard EG, Colmer TD. Plant growth and physiology under heterogeneous salinity. Plant and Soil. 2012; 354(1–2), 1–19. doi: 10.1007/s11104-012-1193-8

17. Feng XH, An P, Guo K, Li XG, Liu XJ, Zhang XM. Growth, root compensation and ion distribution in Lycium chinense under heterogeneous salinity stress. Scientia Horticulturae, 2017; 226, 24–32. doi: 10.1016/j.scienta.2017.08.011

18. Dong HZ, Kong XQ, Luo Z, Li WJ, Xin CS. Unequal salt distribution in the root zone increases growth and yield of cotton. European Journal of Agronomy. 2010; 33(4), 285–292. doi: 10.1016/j.eja.2010.08.002

19. Kong XQ, Luo Z, Dong HZ, Eneji AE, Li WJ. Effects of non-uniform root zone salinity on water use, Na+ recirculation, and Na+ and H+ flux in cotton. Journal of Experimental Botany. 2012; 63(5), 2105–2116. doi: 10.1093/jxb/err420 22200663

20. Sun JJ, Yang GW, Zhang WJ, Zhang YJ. Effects of heterogeneous salinity on growth, water uptake, and tissue ion concentrations of alfalfa. Plant and Soil. 2016; 408(1–2), 211–226. doi: 10.1007/s11104-016-2922-1

21. Klapheck S, Zimmer I, Cosse H. Scavenging of hydrogen peroxide in the endosperm of Ricinus communis by ascorbate peroxidase. Plant and Cell Physiology. 1990; 31(7), 1005–1013. doi: 10.1093/oxfordjournals.pcp.a077996

22. Giannopolitis CN, Ries SK. Superoxide dismutases. I. Occurrence in Higher Plants. Plant Physiology. 1977; 59(2), 309–314. doi: 10.1104/pp.59.2.309 16659839

23. Aebi H. Catalase in vitro. Methods in Enzymology. 1984; 105, 121–126. doi: 10.1016/s0076-6879(84)05016-3 6727660

24. Bagheri M, Gholami M, Baninasab B. Hydrogen peroxide-induced salt tolerance in relation to antioxidant systems in pistachio seedlings. Scientia Horticulturae, 2019; 243(2019), 207–213. doi: 10.1016/j.scienta.2018.08.026

25. Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant and Soil. 1973; 39(1), 205–207. doi: 10.1007/BF00018060

26. Xiong M, Zhang XJ, Shabala S, Shabala L, Chen YJ, Xiang C, et al. Evaluation of salt tolerance and contributing ionic mechanism in nine Hami melon landraces in Xinjiang, China. Scientia Horticulturae. 2018; 237, 277–286. doi: 10.1016/j.scienta.2018.04.023

27. Huang LL, Li MJ, Zhou K, Sun TT, Hu LY, Li CY, et al. Uptake and metabolism of ammonium and nitrate in response to drought stress in Malus prunifolia. Plant Physiol Biochem. 2018; 127, 185–193. doi: 10.1016/j.plaphy.2018.03.031 29609174

28. Zhang H, Yang YZ, Wang CY, Liu M, Li H, Fu Y, et al. Large-scale transcriptome comparison reveals distinct gene activations in wheat responding to stripe rust and powdery mildew. BMC Genomics. 2014; 15(1), 898–912. doi: 10.1186/1471-2164-15-898 25318379

29. Liu XM, Xu X, Li BH, Wang XQ, Wang GQ, Li MR. RNA-seq transcriptome analysis of maize inbred carrying nicosulfuron-tolerant and nicosulfuron-susceptible alleles. International Journal of Molecular Sciences. 2015; 16(12), 5975–5989. doi: 10.3390/ijms16035975 25782159

30. Zhou Y, Yang P, Cui F, Zhang F, Luo X, Xie J. Transcriptome analysis of salt stress responsiveness in the seedlings of Dongxiang wild rice (Oryza rufipogon Griff.). Plos One. 2016; 11(1), e0146242. doi: 10.1371/journal.pone.0146242 26752408

31. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, et al. The Sorghum bicolor genome and the diversification of grasses. Nature. 2009; 457(7229), 551–556. doi: 10.1038/nature07723 19189423

32. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-seq. Bioinformatics. 2009; 25(9), 1105–1111. doi: 10.1093/bioinformatics/btp120 19289445

33. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nature Biotechnology. 2010; 28(5), 511–515. doi: 10.1038/nbt.1621 20436464

34. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology. 2014; 15(12), 550–571. doi: 10.1186/s13059-014-0550-8 25516281

35. Johnson SM, Lim FL, Finkler A, Fromm H, Slabas AR, Knight MR. Transcriptomic analysis of Sorghum bicolor responding to combined heat and drought stress. BMC Genomics. 2014; 15(1), 456–475. doi: 10.1186/1471-2164-15-456 24916767

36. Chen S, Wang ZC, Guo XP, Rasool G, Zhang J, Xie Y, et al. Effects of vertically heterogeneous soil salinity on tomato photosynthesis and related physiological parameters. Scientia Horticulturae. 2019; 249, 120–130. doi: 10.1016/j.scienta.2019.01.049

37. Bazihizina N, Barrett-Lennard EG, Colmer TD. Plant responses to heterogeneous salinity: Growth of the halophyte Atriplex nummularia is determined by the root-weighted mean salinity of the root zone. Journal of Experimental Botany. 2012; 63(18), 6347–6358. doi: 10.1093/jxb/ers302 23125356

38. Kong XQ, Luo Z, Dong HZ, Eneji AE, Li WJ. H2O2 and ABA signaling are responsible for the increased Na+ efflux and water uptake in Gossypium hirsutum L. roots in the non-saline side under non-uniform root zone salinity. Journal of Experimental Botany. 2016; 67(8), 2247–2261. doi: 10.1093/jxb/erw026 26862153

39. Xiong X, Liu N, Wei YQ, Bi YX, Luo JC, Xu RX et al. Effects of non-uniform root zone salinity on growth, ion regulation, and antioxidant defense system in two alfalfa cultivars. Plant Physiology and Biochemistry. 2018; 132, 434–444. doi: 10.1016/j.plaphy.2018.09.028 30290335

40. Varela ALN, Oliveira JTA, Komatsu S, Silva RGG, Martins TF, Souza PFN, et al. A resistant cowpea [Vigna unguiculata (L.) Walp.] genotype became susceptible to cowpea severe mosaic virus (CPSMV) after exposure to salt stress. Journal of Proteomics. 2019; 194, 200–217. doi: 10.1016/j.jprot.2018.11.015 30471437

41. Yang H, Shukla MK, Mao XM, Kang SZ, Du TS. Interactive regimes of reduced irrigation and salt stress depressed tomato water use efficiency at leaf and plant scales by affecting leaf physiology and stem sap flow. Frontiers in Plant Science. 2019; 10, 160–177. doi: 10.3389/fpls.2019.00160 30873187

42. Abid MA, Liang CZ, Malik W, Meng ZG, Tao ZH, Meng Z, et al. Cascades of ionic and molecular networks involved in expression of genes underpin salinity tolerance in cotton. Journal of Plant Growth Regulation. 2018; 37(2), 668–679. doi: 10.1007/s00344-017-9744-0

43. Deinlein U, Stephan AB, Horie T, Luo W, Xu GH, Schroeder JI. Plant salt-tolerance mechanisms. Trends in Plant Science. 2014; 19(6), 371–379. doi: 10.1016/j.tplants.2014.02.001 24630845

44. Ali A, Yun D. Salt stress tolerance: What do we learn from halophytes? Journal of Plant Biology. 2017; 60(5), 431–439. doi: 10.1007/s12374-017-0133-9

45. Jin HX, Dong DK, Yang QH, Zhu DH. Salt-responsive transcriptome profiling of Suaeda glauca via RNA sequencing. Plos One. 2016; 11(3), e0150504. doi: 10.1371/journal.pone.0150504 26930632

46. Lin J, Li J, Yuan F, Yang Z, Wang B, Chen M. Transcriptome profiling of genes involved in photosynthesis in Elaeagnus angustifolia L. under salt stress. Photosynthetica. 2018; 56(4), 998–1009. doi: 10.1007/s11099-018-0824-6

47. Ashraf M, Harris PJC. Photosynthesis under stressful environments: An overview. Photosynthetica. 2013; 51(2), 163–190. doi: 10.1007/s11099-013-0021-6

48. Anjula C, Ashu S, Sengar RS. Antioxidant activity in rice under salinity stress: An overview. Plant Archives. 2015; 15(1), 7–13.

49. Per TS, Khan NA, Reddy PS, Masood A, Hasanuzzaman M, Khan MIR, et al. Approaches in modulating proline metabolism in plants for salt and drought stress tolerance: Phytohormones, mineral nutrients and transgenics. Plant Physiology and Biochemistry. 2017; 115, 126–140. doi: 10.1016/j.plaphy.2017.03.018 28364709

50. Amorim LLB, Ferreira-Neto JRC, Bezerra-Neto JP, Pandolfi V, de Araujo FT, Matos MKD, et al. Cowpea and abiotic stresses: identification of reference genes for transcriptional profiling by qPCR. Plant Methods. 2018; 14(1), 88–105. doi: 10.1186/s13007-018-0354-z 30337949

51. Ibrahim W, Zhu YM, Chen Y, Qiu CW, Zhu SJ, Wu FB. Genotypic differences in leaf secondary metabolism, plant hormones and yield under alone and combined stress of drought and salinity in cotton genotypes. Physiologia Plantarum. 2019; 165(2), 343–355. doi: 10.1111/ppl.12862 30367694

52. Lu SP, Bahn SC, Qu G, Qin HY, Hong Y, Xu QP, et al. Increased expression of phospholipase D1 in guard cells decreases water loss with improved seed production under drought in Brassica napus. Plant Biotechnology Journal. 2013; 11(3), 380–389. doi: 10.1111/pbi.12028 23279050

53. Chen HY, Yu XM, Zhang XD, Yang L, Huang X, Zhang J, et al. Phospholipase D1-mediated phosphatidic acid change is a key determinant of desiccation-induced viability loss in seeds. Plant Cell and Environment. 2018; 41(1), 50–63. doi: 10.1111/pce.12925 28152567

54. Zhang JH, Jia WS, Yang JC, Ismail AM. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Research. 2006; 97(1), 111–119. doi: 10.1016/j.fcr.2005.08.018

55. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR. Specific oxidative cleavage of carotenoids by VP14 of maize. Science. 1997; 276(5320), 1872–1874. doi: 10.1126/science.276.5320.1872 9188535

56. Kriechbaumer V, Park WJ, Gierl A, Glawischnig E. Auxin biosynthesis in maize. Plant Biology. 2006; 8(3), 334–339. doi: 10.1055/s-2006-923883 16807825

57. Mano Y, Nemoto K. The pathway of auxin biosynthesis in plants. Journal of Experimental Botany. 2012; 63(8), 2853–2872. doi: 10.1093/jxb/ers091 22447967

58. Seo M, Akaba S, Oritani T, Delarue M, Bellini C, Caboche M, et al. Higher activity of an aldehyde oxidase in the auxin-overproducing superroot1 mutant of Arabidopsis thaliana. Plant Physiology. 1998; 116(2), 687–693. doi: 10.1104/pp.116.2.687 9489015

59. Kollath-Leiss K, Bonniger C, Sardar P, Kempken F. BEM46 shows eisosomal localization and association with tryptophan-derived auxin pathway in Neurospora crassa. Eukaryotic Cell. 2014; 13(8), 1051–1063. doi: 10.1128/EC.00061-14 24928924

60. Yin HJ, Li MZ, Li DD, Khan SA, Hepworth SR, Wang SM. Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte. BMC Plant Biology. 2019; 19(1), 88–103. doi: 10.1186/s12870-019-1686-1 30819118

61. Sergiev I, Todorova D, Shopova E, Jankauskiene J, Jankovska-Bortkevic E, Jurkoniene S. Exogenous auxin type compounds amend PEG-induced physiological responses of pea plants. Scientia Horticulturae. 2019; 248, 200–205. doi: 10.1016/j.scienta.2019.01.015

62. Wang J, Huang RF. Modulation of ethylene and ascorbic acid on reactive oxygen species scavenging in plant salt response. Frontiers in Plant Science. 2019; 10, 319–325. doi: 10.3389/fpls.2019.00319 30936887

63. Bernal-Vicente A, Cantabella D, Petri C, Hernandez JA, Diaz-Vivancos P. The salt-stress response of the transgenic plum line J8-1 and its interaction with the salicylic acid biosynthetic pathway from mandelonitrile. International Journal of Molecular Sciences. 2018; 19, 3519–3538. doi: 10.3390/ijms19113519 30413110

64. Boro P, Sultana A, Mandal K, Chattopadhyay S. Transcriptomic changes under stress conditions with special reference to glutathione contents. Nucleus-India. 2018; 61(3), 241–252. doi: 10.1007/s13237-018-0256-5

65. Ghassmi-Golezani K, Farhangi-Abriz S. Foliar sprays of salicylic acid and jasmonic acid stimulate H+-ATPase activity of tonoplast, nutrient uptake and salt tolerance of soybean. Ecotoxicology and Environmental Safety. 2018; 166, 18–25. doi: 10.1016/j.ecoenv.2018.09.059 30240931

66. Sobajima H, Tani T, Chujo T, Okada K, Suzuki K, Mori S, et al. Identification of a jasmonic acid-responsive region in the promoter of the rice 12-oxophytodienoic acid reductase 1 gene OsOPR1. Bioscience Biotechnology and Biochemistry. 2007; 71(12), 3110–3115. doi: 10.1271/bbb.70532 18071256

67. Liu ZQ, Shi LP, Liu YY, Tang Q, Shen L, Yang S, et al. Genome-wide identification and transcriptional expression analysis of mitogen-activated protein kinase and mitogen-activated protein kinase kinase genes in Capsicum annuum. Frontiers in Plant Science. 2015; 6, 780–801. doi: 10.3389/fpls.2015.00780 26442088

68. Xing Y, Chen WH, Jia WS, Zhang JH. Mitogen-activated protein kinase kinase 5 (MKK5)-mediated signalling cascade regulates expression of iron superoxide dismutase gene in Arabidopsis under salinity stress. Journal of Experimental Botany. 2015; 66(19), 5971–5981. doi: 10.1093/jxb/erv305 26136265

69. Haddadi P, Ma LS, Wang HY, Borhan MH. Genome-wide transcriptomic analyses provide insights into the lifestyle transition and effector repertoire of Leptosphaeria maculans during the colonization of Brassica napus seedlings. Molecular Plant Pathology. 2016; 17(8), 1196–1210. doi: 10.1111/mpp.12356 26679637

70. Secchi F, Lovisolo C, Schubert A. Expression of OePIP2.1 aquaporin gene and water relations of Olea europaea twigs during drought stress and recovery. Annals of Applied Biology. 2007; 150(2), 163–167. doi: 10.1111/j.1744-7348.2007.00118.x

71. Mahdieh M, Mostajeran A, Horie T, Katsuhara M. Drought stress alters water relations and expression of PIP-type aquaporin genes in Nicotiana tabacum Plants. Plant and Cell Physiology. 2008; 49(5), 801–813. doi: 10.1093/pcp/pcn054 18385163

72. Molina C, Rotter B, Horres R, Udupa SM, Besser B, Bellarmino L, et al. SuperSAGE: The drought stress-responsive transcriptome of chickpea roots. BMC Genomics. 2008; 9, 553–581. doi: 10.1186/1471-2164-9-553 19025623

73. Galmes J, Pou A, Alsina MM, Tomas M, Medrano H, Flexas J. Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): Relationship with ecophysiological status. Planta. 2007; 226(3), 671–681. doi: 10.1007/s00425-007-0515-1 17447082

74. Golldack D, Luking I, Yang O. Plant tolerance to drought and salinity: Stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Reports. 2011; 30(8), 1383–1391. doi: 10.1007/s00299-011-1068-0 21476089

75. Khan SA, Li MZ, Wang SM, Yin HJ. Revisiting the role of plant transcription factors in the battle against abiotic stress. International Journal of Molecular Sciences. 2018; 19, 1634–1633. doi: 10.3390/ijms19061634 29857524

76. Lata C, Yadav A, Prasad M. Role of plant transcription factors in abiotic stress tolerance. In: Shanker A, Venkateswarlu B, editors. Abiotic stress response in plants—physiological, biochemical and genetic perspectives. India: IntechOpen; 2011. pp. 269–296.

77. Zhang SC, Yang RY, Huo YQ, Liu SS, Yang GD, Huang JG, et al. Expression of cotton PLATZ1 in transgenic Arabidopsis reduces sensitivity to osmotic and salt stress for germination and seedling establishment associated with modification of the abscisic acid, gibberellin, and ethylene signaling pathways. BMC Plant Biology. 2018; 18(1), 218–229. doi: 10.1186/s12870-018-1416-0 30286716

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