Cited by 14Spaceflight effects on biologyTelomeres, Telomerase, and SenescencePlant Stress Responses and Tolerance

Telomere dynamics and oxidative stress in Arabidopsis grown in lunar regolith simulant

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Barcenilla, Borja Barbero, Kundel, Ishan, Hall, Emily, Hilty, Nicolas, Ulianich, Pavel, Cook, Jillian, Turley, Jake, Yerram, Monisha +3 more·2024·Frontiers in Plant Science

Abstract

NASA envisions a future where humans establish a thriving colony on the Moon by 2050. Plants will be essential for this endeavor, but little is known about their adaptation to extraterrestrial bodies. The capacity to grow plants in lunar regolith would represent a major step towards this goal by minimizing the reliance on resources transported from Earth. Recent studies reveal that Arabidopsis thaliana can germinate and grow on genuine lunar regolith as well as on lunar regolith simulant. However, plants arrest in vegetative development and activate a variety of stress response pathways, most notably the oxidative stress response. Telomeres are hotspots for oxidative damage in the genome and a marker of fitness in many organisms. Here we examine A. thaliana growth on a lunar regolith simulant and the impact of this resource on plant physiology and on telomere dynamics, telomerase enzyme activity and genome oxidation. We report that plants successfully set seed and generate a viable second plant generation if the lunar regolith simulant is pre-washed with an antioxidant cocktail. However, plants sustain a higher degree of genome oxidation and decreased biomass relative to conventional Earth soil cultivation. Moreover, telomerase activity substantially declines and telomeres shorten in plants grown in lunar regolith simulant, implying that genome integrity may not be sustainable over the long-term. Overcoming these challenges will be an important goal in ensuring success on the lunar frontier.

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Crossref · 10.3389/fpls.2024.1351613

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  • Growth rates in regolith simulants tend to be slower and plants often exhibit signs of phenotypic stress.

    “However, growth rates tend to be slower, and plants often exhibit signs of phenotypic stress (Paul et al., 2022), including a decline in telomere dynamics and a loss of sustainable genome integrity (Barcenilla et al., 2024).”

    From Spirulina supported plant growth in regolith simulants and elevated levels of CO2 (2025) · cites this paper as Barcenilla et al., 2024

    The Results report shorter telomeres and reduced telomerase activity in Arabidopsis grown in lunar regolith simulant. The paper describes long-term genome integrity as potentially unsustainable, not as an observed loss. The slower growth and phenotypic stress in the citing sentence are attributed to Paul et al. (2022), not to this source. (LLM, conf=0.86)

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  1. Adam R. Díez-González L. Ocaña A. Šeruga B. Amir E. Templeton A. J. (2017). Prognostic role of telomere length in Malignancies: A meta-analysis and meta-regression. Exp. Mol. Pathol. 102, 455– 474. doi: 10.1016/j.yexmp.2017.05.010 28506770 · DOI
  2. Ahmed S. Passos J. F. Birket M. J. Beckmann T. Brings S. Peters H.. (2008). Telomerase does not counteract telomere shortening but protects mitochondrial function under oxidative stress. J. Cell Sci. 121, 1046– 1053. doi: 10.1242/jcs.019372 18334557 · DOI
  3. Ahmed W. Lingner J. (2018a). PRDX1 and MTH1 cooperate to prevent ROS-mediated inhibition of telomerase. Genes Dev. 32, 658– 669. doi: 10.1101/gad.313460.118 29773556 PMC6004070 · DOI
  4. Ahmed W. Lingner J. (2018b). Impact of oxidative stress on telomere biology. Differentiation 99, 21– 27. doi: 10.1016/j.diff.2017.12.002 29274896 · DOI · Paper page
  5. Armstrong S. J. Sanchez-Moran E. Franklin F. C. H. (2009). Cytological analysis of Arabidopsis thaliana meiotic chromosomes. Methods Mol. Biol. 558, 131– 145. doi: 10.1007/978-1-60761-103-5_9 19685323 · DOI
  6. Asghar M. Hasselquist D. Hansson B. Zehtindjiev P. Westerdahl H. Bensch S. (2015). Hidden costs of infection: Chronic malaria accelerates telomere degradation and senescence in wild birds. Science 347, 436– 438. doi: 10.1126/science.1261121 25613889 · DOI
  7. Bains S. K. Chapman K. Bright S. Senan A. Kadhim M. Slijepcevic P. (2019). Effects of ionizing radiation on telomere length and telomerase activity in cultured human lens epithelium cells. Int. J. Radiat. Biol. 95, 54– 63. doi: 10.1080/09553002.2018.1466066 29667481 · DOI
  8. Barbero Barcenilla B. Shippen D. E. (2019). Back to the future: The intimate and evolving connection between telomere-related factors and genotoxic stress. J. Biol. Chem. 294, 14803– 14813. doi: 10.1074/jbc.AW119.008145 31434740 PMC6779425 · DOI
  9. Barcenilla B. B. Meyers A. D. Castillo-González C. Young P. Min J.-H. Song J.. (2023). Arabidopsis telomerase takes off by uncoupling enzyme activity from telomere length maintenance in space. Nat. Commun. 14, 7854. doi: 10.1038/s41467-023-41510-4 38030615 PMC10686995 · DOI
  10. Barnes R. P. Fouquerel E. Opresko P. L. (2019). The impact of oxidative DNA damage and stress on telomere homeostasis. Mech. Ageing Dev. 177, 37– 45. doi: 10.1016/j.mad.2018.03.013 29604323 PMC6162185 · DOI
  11. Bauch C. Becker P. H. Verhulst S. (2014). Within the genome, long telomeres are more informative than short telomeres with respect to fitness components in a long-lived seabird. Mol. Ecol. 23, 300– 310. doi: 10.1111/mec.12602 24274429 · DOI
  12. Borghini A. Faita F. Mercuri A. Minichilli F. Bustaffa E. Bianchi F.. (2016). Arsenic exposure, genetic susceptibility and leukocyte telomere length in an Italian young adult population. Mutagenesis 31, 539– 546. doi: 10.1093/mutage/gew017 27084675 · DOI
  13. Bose S. Suescún A. V. Song J. Castillo-González C. Behailu B. A. Branham E.. (2020). tRNA ADENOSINE DEAMINASE 3 is required for telomere maintenance in Arabidopsis thaliana. Plant Cell Rep. 39, 1669– 1685. doi: 10.1007/s00299-020-02594-0 32959123 PMC7655638 · DOI
  14. Braddock M. (2021). “ Understanding and managing the hazards and opportunities of lunar regolith in greenhouse agriculture.” in The Human Factor in the Settlement of the Moon. Eds. M. B. Rappaport and K. Szocik. (Springer, Cham: Space and Society), 97– 114. doi: 10.1007/978-3-030-81388-8_6 · DOI
  15. Campitelli B. E. Razzaque S. Barbero B. Abdulkina L. R. Hall M. H. Shippen D. E.. (2021). Plasticity, pleiotropy and fitness trade-offs in Arabidopsis genotypes with different telomere lengths. New Phytol. 233, 1939– 1952. doi: 10.1111/nph.17880 34826163 PMC9218941 · DOI
  16. Carrier W. D. Mitchell J. K. Mahmood A. (1973). The nature of lunar soil. J. Soil Mech. Found. 99, 813– 832. doi: 10.1061/JSFEAQ.0001935 · DOI
  17. Castillo-González C. Barcenilla B. B. Young P. G. Hall E. Shippen D. E. (2022). Quantification of 8-oxoG in plant telomeres. Int. J. Mol. Sci. 23, 4990. doi: 10.3390/ijms23094990 35563379 PMC9102096 · DOI
  18. Cheng Y. Liu P. Lu Z. Guan J. Correspondence G. W. Zheng Q.. (2018). Mitochondrial trafficking and processing of telomerase RNA TERC. Cell Rep. 24, 2589– 2595. doi: 10.1016/j.celrep.2018.08.003 30184494 · DOI
  19. Coluzzi E. Leone S. Sgura A. (2019). Oxidative stress induces telomere dysfunction and senescence by replication fork arrest. Cells 8, 19. doi: 10.3390/cells8010019 30609792 PMC6356380 · DOI · Paper page
  20. Cuypers A. Plusquin M. Remans T. Jozefczak M. Keunen E. Gielen H.. (2010). Cadmium stress: an oxidative challenge. BioMetals 23, 927– 940. doi: 10.1007/s10534-010-9329-x 20361350 · DOI
  21. Doyle J. J. Doyle J. L. (1987). A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19, 11– 15.
  22. El-Beltagi H. S. Mohamed H. I. Sofy M. R. (2020). Role of ascorbic acid, glutathione and proline applied as single or in sequence combination in improving chickpea plant through physiological change and antioxidant defense under different levels of irrigation intervals. Molecules 25 (7), 1702. doi: 10.3390/molecules25071702 32276352 PMC7180974 · DOI
  23. Epel E. S. Blackburn E. H. Lin J. Dhabhar F. S. Adler N. E. Morrow J. D.. (2004). Accelerated telomere shortening in response to life stress. Proc. Natl. Acad. Sci. 101, 17312– 17315. doi: 10.1073/pnas.0407162101 15574496 PMC534658 · DOI · Paper page
  24. Fillman T. Shimizu-Furusawa H. Ng C. F. S. Parajuli R. P. Watanabe C. (2016). Association of cadmium and arsenic exposure with salivary telomere length in adolescents in Terai, Nepal. Environ. Res. 149, 8– 14. doi: 10.1016/j.envres.2016.04.037 27155138 · DOI
  25. Fitzgerald M. S. Riha K. Gao F. Ren S. McKnight T. D. Shippen D. E. (1999). Disruption of the telomerase catalytic subunit gene from Arabidopsis inactivates telomerase and leads to a slow loss of telomeric DNA. Proc. Natl. Acad. Sci. U. S. A. 96, 14813– 14818. doi: 10.1073/pnas.96.26.14813 10611295 PMC24730 · DOI
  26. Flora S. J. S. (2002). Nutritional components modify metal absorption, toxic response and chelation therapy. J. Nutr. Environ. Med. 12, 53– 67. doi: 10.1080/13590840220123361 · DOI
  27. Fouquerel E. Lormand J. Bose A. Lee H.-T. Kim G. S. Li J.. (2016). Oxidative guanine base damage regulates human telomerase activity. Nat. Struct. Mol. Biol. 23, 1092– 1100. doi: 10.1038/nsmb.3319 27820808 PMC5140714 · DOI · Paper page
  28. Garrett-Bakelman F. E. Darshi M. Green S. J. Gur R. C. Lin L. Macias B. R.. (2019). The NASA Twins Study: A multidimensional analysis of a year-long human spaceflight. Science 364, 6436. doi: 10.1126/science.aau8650 PMC7580864 30975860 · DOI · Paper page
  29. Gonzales-Ebsen A. C. Gregersen N. Olsen R. K. (2017). Linking telomere loss and mitochondrial dysfunction in chronic disease. Front. Biosci. 22, 117– 127. doi: 10.2741/4475 27814605 · DOI
  30. González-García M.-P. Pavelescu I. Canela A. Sevillano X. Leehy K. A. Nelson A. D. L.. (2015). Single-cell telomere-length quantification couples telomere length to meristem activity and stem cell development in Arabidopsis. Cell Rep. 11, 977– 989. doi: 10.1016/j.celrep.2015.04.013 25937286 PMC4827700 · DOI
  31. Gul N. Ahmad P. Wani T. A. Tyagi A. Aslam S. (2022). Glutathione improves low temperature stress tolerance in pusa sheetal cultivar of Solanum lycopersicum. Sci. Rep. 12, 12548. doi: 10.1038/s41598-022-16440-8 35869119 PMC9307597 · DOI
  32. Guo S. Ma X. Cai W. Wang Y. Gao X. Fu B.. (2022). Exogenous proline improves salt tolerance of alfalfa through modulation of antioxidant capacity, ion homeostasis, and proline metabolism. Plants 11, 2994. doi: 10.3390/plants11212994 36365447 PMC9657615 · DOI
  33. Haussmann M. F. Mauck R. A. (2008). Telomeres and longevity: testing an evolutionary hypothesis. Mol. Biol. Evol. 25, 220– 228. doi: 10.1093/molbev/msm244 18071200 · DOI
  34. Haussmann M. F. Winkler D. W. Vleck C. M. (2005). Longer telomeres associated with higher survival in birds. Biol. Lett. 1, 212– 214. doi: 10.1098/rsbl.2005.0301 17148169 PMC1626238 · DOI
  35. Heacock M. Spangler E. Riha K. Puizina J. Shippen D. E. (2004). Molecular analysis of telomere fusions in Arabidopsis: Multiple pathways for chromosome end-joining. EMBO J. 23, 2304– 2313. doi: 10.1038/sj.emboj.7600236 15141167 PMC419913 · DOI
  36. Jaishankar M. Tseten T. Anbalagan N. Mathew B. B. Beeregowda K. N. (2014). Toxicity, mechanism and health effects of some heavy metals. Interdiscip. Toxicol. 7, 60– 72. doi: 10.2478/intox-2014-0009 26109881 PMC4427717 · DOI · Paper page
  37. Kannan K. Nelson A. D. L. Shippen D. E. (2008). Dyskerin Is a component of the Arabidopsis telomerase RNP required for telomere maintenance. Mol. Cell. Biol. 28, 2332– 2341. doi: 10.1128/MCB.01490-07 18212040 PMC2268427 · DOI
  38. Kasiviswanathan P. Swanner E. D. Halverson L. J. Vijayapalani P. (2022). Farming on Mars: Treatment of basaltic regolith soil and briny water simulants sustains plant growth. PloS One 17, e0272209. doi: 10.1371/journal.pone.0272209 35976812 PMC9385024 · DOI
  39. Kibinza S. Bazin J. Bailly C. Farrant J. M. Corbineau F. El-Maarouf-Bouteau H. (2011). Catalase is a key enzyme in seed recovery from ageing during priming. Plant Sci. 181, 309– 315. doi: 10.1016/j.plantsci.2011.06.003 21763542 · DOI
  40. Kim M. S. Koo N. Kim J. G. Lee S. H. (2021). Effects of washing solution, washing time, and solid-solution rate on the maximum heavy metals removal efficiency. Appl. Sci. 11, 6398. doi: 10.3390/app11146398 · DOI
  41. Kurz D. J. Decary S. Hong Y. Trivier E. Akhmedov A. Erusalimsky J. D. (2004). Chronic oxidative stress compromises telomere integrity and accelerates the onset of senescence in human endothelial cells. J. Cell Sci. 117, 2417– 2426. doi: 10.1242/jcs.01097 15126641 · DOI · Paper page
  42. Lee H.-T. Bose A. Lee C.-Y. Opresko P. L. Myong S. (2017). Molecular mechanisms by which oxidative DNA damage promotes telomerase activity. Nucleic Acids Res. 45, 11752– 11765. doi: 10.1093/nar/gkx789 28981887 PMC5714237 · DOI
  43. Lee J. R. Xie X. Yang K. Zhang J. Lee S. Y. Shippen D. E. (2016). Dynamic interactions of Arabidopsis TEN1: Stabilizing telomeres in response to heat stress. Plant Cell 28, 2212– 2224. doi: 10.1105/tpc.16.00408 27609839 PMC5059806 · DOI
  44. Leehy K. A. Lee J. R. Song X. Renfrew K. B. Shippen D. E. (2013). MERISTEM DISORGANIZATION1 encodes TEN1, an essential telomere protein that modulates telomerase processivity in Arabidopsis. Plant Cell 25, 1343– 1354. doi: 10.1105/tpc.112.107425 23572541 PMC3663272 · DOI
  45. Lim C. J. Cech T. R. (2021). Shaping human telomeres: from shelterin and CST complexes to telomeric chromatin organization. Nat. Rev. Mol. Cell Biol. 22, 283– 2021. doi: 10.1038/s41580-021-00328-y 33564154 PMC8221230 · DOI
  46. Liu Y. Park J. Schnare D. Hill E. Taylor L. A. (2008). Characterization of lunar dust for toxicological studies: texture and shape characteristics. J. Aerosp. Eng. 21, 272– 279. doi: 10.1061/(ASCE)0893-1321(2008)21:4(272) · DOI
  47. Luxton J. J. McKenna M. J. Lewis A. Taylor L. E. George K. A. Dixit S. M.. (2020b). Telomere length dynamics and DNA damage responses associated with long-duration spaceflight. Cell Rep. 33, 108457. doi: 10.1016/j.celrep.2020.108457 33242406 · DOI
  48. Luxton J. J. McKenna M. J. Lewis A. M. Taylor L. E. Jhavar S. G. Swanson G. P.. (2021). Telomere length dynamics and chromosomal instability for predicting individual radiosensitivity and risk via machine learning. J. Pers. Med. 11, 188. doi: 10.3390/jpm11030188 33800260 PMC8002073 · DOI
  49. Luxton J. J. McKenna M. J. Taylor L. E. George K. A. Zwart S. R. Crucian B. E.. (2020a). Temporal telomere and DNA damage responses in the space radiation environment. Cell Rep. 33, 108435. doi: 10.1016/j.celrep.2020.108435 33242411 · DOI
  50. Lyčka M. Peska V. Demko M. Spyroglou I. Kilar A. Fajkus J.. (2021). WALTER: an easy way to online evaluate telomere lengths from terminal restriction fragment analysis. BMC Bioinf. 22, 145. doi: 10.1186/s12859-021-04064-0 PMC7986547 33752601 · DOI
  51. Meyers A. Wyatt S. E. (2022). Plant space biology in the genomics age. Annu. Plant Rev. 5, 123– 150. doi: 10.1002/9781119312994.apr0784 · DOI
  52. Ming D. W. Henninger D. L. (1994). Use of lunar regolith as a substrate for plant growth. Adv. Sp. Res. 14, 435– 443. doi: 10.1016/0273-1177(94)90333-6 11538023 · DOI
  53. National Academies of Sciences and Medicine (2023). Origins, worlds, and life: A decadal strategy for planetary science and astrobiology 2023-2032 (Washington, DC: The National Academies Press).
  54. Oikawa S. Kawanishi S. (1999). Site-specific DNA damage at GGG sequence by oxidative stress may accelerate telomere shortening. FEBS Lett. 453, 365– 368. doi: 10.1016/S0014-5793(99)00748-6 10405177 · DOI · Paper page
  55. Paul A.-L. Elardo S. M. Ferl R. (2022). Plants grown in Apollo lunar regolith present stress-associated transcriptomes that inform prospects for lunar exploration. Commun. Biol. 5, 382. doi: 10.1038/s42003-022-03334-8 35552509 PMC9098553 · DOI · Paper page
  56. Pawlas N. Płachetka-Bozek A. Kozlłowska A. Mikolłajczyk A. Kasperczyk A. Dobrakowski M.. (2015). Telomere length, telomerase expression, and oxidative stress in lead smelters. Toxicol. Ind. Heal. 32, 1961– 1970. doi: 10.1177/0748233715601758 26381690 · DOI
  57. Pinzaru A. M. Hom R. A. Beal A. Phillips A. F. Ni E. Cardozo T.. (2016). Telomere replication stress induced by POT1 inactivation accelerates tumorigenesis. Cell Rep. 15, 2170– 2184. doi: 10.1016/j.celrep.2016.05.008 27239034 PMC6145145 · DOI
  58. Protsenko E. Rehkopf D. Prather A. A. Epel E. Lin J. (2020). Are long telomeres better than short? Relative contributions of genetically predicted telomere length to neoplastic and non-neoplastic disease risk and population health burden. PloS One 15, e0240185. doi: 10.1371/journal.pone.0240185 33031470 PMC7544094 · DOI
  59. Renfrew K. B. Song X. Lee J. R. Arora A. Shippen D. E. (2014). POT1a and components of CST engage telomerase and regulate its activity in Arabidopsis. PloS Genet. 10, e1004738. doi: 10.1371/journal.pgen.1004738 25329641 PMC4199523 · DOI
  60. Riha K. McKnight T. D. Griffing L. R. Shippen D. E. (2001). Living with genome instability: Plant responses to telomere dysfunction. Science 291, 1797– 1800. doi: 10.1126/science.1057110 11230697 · DOI
  61. Santos J. H. Meyer J. N. Skorvaga M. Annab L. A. Van Houten B. (2004). Mitochondrial hTERT exacerbates free-radical-mediated mtDNA damage. Aging Cell 3, 399– 411. doi: 10.1111/j.1474-9728.2004.00124.x 15569357 · DOI
  62. Santos J. H. Meyer J. N. Van Houten B. (2006). Mitochondrial localization of telomerase as a determinant for hydrogen peroxide-induced mitochondrial DNA damage and apoptosis. Hum. Mol. Genet. 15, 1757– 1768. doi: 10.1093/hmg/ddl098 16613901 · DOI
  63. Sarkar J. Liu Y. (2016). The origin of oxidized guanine resolves the puzzle of oxidation-induced telomere-length alterations. Nat. Struct. Mol. Biol. 23, 1070– 1071. doi: 10.1038/nsmb.3332 27922610 PMC5819590 · DOI
  64. Shakirov E. V. Shippen D. E. (2004). Length regulation and dynamics of individual telomere tracts in wild-type Arabidopsis. Plant Cell 16, 1959– 1967. doi: 10.1105/tpc.104.023093 15258263 PMC519188 · DOI
  65. Sharma P. Jha A. B. Dubey R. S. Pessarakli M. (2012). Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J. Bot. 2012, 1– 26. doi: 10.1155/2012/217037 · DOI
  66. Shay J. W. Wright W. E. (2019). Telomeres and telomerase: three decades of progress. Nat. Rev. Genet. 20, 299– 309. doi: 10.1038/s41576-019-0099-1 30760854 · DOI · Paper page
  67. Song X. Leehy K. Warrington R. T. Lamb J. C. Surovtseva Y. V. Shippen D. E. (2008). STN1 protects chromosome ends in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U. S. A. 105, 19815– 19820. doi: 10.1073/pnas.0807867105 19064932 PMC2604966 · DOI
  68. Song J. Logeswaran D. Castillo-González C. Li Y. Bose S. Aklilu B. B.. (2019). The conserved structure of plant telomerase RNA provides the missing link for an evolutionary pathway from ciliates to humans. Proc. Natl. Acad. Sci. U. S. A. 116, 24542– 24550. doi: 10.1073/pnas.1915312116 31754031 PMC6900512 · DOI
  69. Stindl R. (2004). Is telomere erosion a mechanism of species extinction? J. Exp. Zool. Part B. Mol. Dev. Evol. 302B, 111– 120. doi: 10.1002/jez.b.20006 15054855 · DOI
  70. Stone R. C. Horvath K. Kark J. D. Susser E. Tishkoff S. A. Aviv A. (2016). Telomere length and the cancer–atherosclerosis trade-off. PloS Genet. 12, e1006144. doi: 10.1371/journal.pgen.1006144 27386863 PMC4936693 · DOI
  71. Surovtseva Y. V. Churikov D. Boltz K. A. Song X. Lamb J. C. Warrington R.. (2009). Conserved Telomere Maintenance Component 1 interacts with STN1 and maintains chromosome ends in higher eukaryotes. Mol. Cell 36, 207– 218. doi: 10.1016/j.molcel.2009.09.017 19854131 PMC2768651 · DOI
  72. Tague B. W. Mantis J. (2006). In planta Agrobacterium-mediated transformation by vacuum infiltration. Methods Mol. Biol. 323, 215– 223. doi: 10.1385/1-59745-003-0:215 16739579 · DOI
  73. Voghel G. Thorin-Trescases N. Mamarbachi A. M. Villeneuve L. Mallette F. A. Ferbeyre G.. (2010). Endogenous oxidative stress prevents telomerase-dependent immortalization of human endothelial cells. Mech. Ageing Dev. 131, 354– 363. doi: 10.1016/j.mad.2010.04.004 20399802 PMC3700881 · DOI
  74. Wai K. M. Swe T. Myar M. T. Aisyah C. R. Hninn T. S. S. (2023). Telomeres susceptibility to environmental arsenic exposure: Shortening or lengthening? Front. Public Heal. 10, 1059248. doi: 10.3389/fpubh.2022.1059248 PMC9871564 36703827 · DOI
  75. Wai K. M. Umezaki M. Umemura M. Mar O. Watanabe C. (2020). Protective role of selenium in the shortening of telomere length in newborns induced by in utero heavy metal exposure. Environ. Res. 183, 109202. doi: 10.1016/j.envres.2020.109202 32045728 · DOI
  76. Wang G. Ren Y. Bai X. Su Y. Han J. (2022). Contributions of beneficial microorganisms in soil remediation and quality improvement of medicinal plants. Plants 11, 3200. doi: 10.3390/plants11233200 36501240 PMC9740990 · DOI
  77. Wang Z. Rhee D. B. Lu J. Bohr C. T. Zhou F. Vallabhaneni H.. (2010). Characterization of oxidative guanine damage and repair in mammalian telomeres. PloS Genet. 6, 28. doi: 10.1371/journal.pgen.1000951 PMC2869316 20485567 · DOI
  78. Weihe A. (2014). Quantification of organellar DNA and RNA using real-time PCR. Methods Mol. Biol. 1132, 235– 243. doi: 10.1007/978-1-62703-995-6_14 24599857 · DOI
  79. Xie X. He Z. Chen N. Tang Z. Wang Q. Cai Y. (2019). The roles of environmental factors in regulation of oxidative stress in plant. BioMed. Res. Int. 2019, 1– 11. doi: 10.1155/2019/9732325 PMC6530150 31205950 · DOI
  80. Xu J. Liu C. Hsu P. C. Zhao J. Wu T. Tang J.. (2019). Remediation of heavy metal contaminated soil by asymmetrical alternating current electrochemistry. Nat. Commun. 101 (10), 1– 8. doi: 10.1038/s41467-019-10472-x PMC6547649 31164649 · DOI
  81. Yan A. Wang Y. Tan S. N. Mohd Yusof M. L. Ghosh S. Chen Z. (2020). Phytoremediation: a promising approach for revegetation of heavy metal-polluted land. Front. Plant Sci. 11, 359. doi: 10.3389/fpls.2020.00359 32425957 PMC7203417 · DOI · Paper page
  82. Zhao Y. Lai K. Cheung I. Youds J. Tarailo M. Tarailo S.. (2006). A mutational analysis of Caenorhabditis elegans in space. Mutat. Res. Fundam. Mol. Mech. Mutagen. 601, 19– 29. doi: 10.1016/j.mrfmmm.2006.05.001 16765996 · DOI
  83. Zhou J. Liu M. Fleming A. M. Burrows C. J. Wallace S. S. (2013). Neil3 and NEIL1 DNA glycosylases remove oxidative damages from quadruplex DNA and exhibit preferences for lesions in the telomeric sequence context. J. Biol. Chem. 288, 27263– 27272. doi: 10.1074/jbc.M113.479055 23926102 PMC3779722 · DOI
  84. Zota A. R. Needham B. L. Blackburn E. H. Lin J. Park S. K. Rehkopf D. H.. (2015). Associations of cadmium and lead exposure with leukocyte telomere length: findings from National Health and Nutrition examination survey 1999–2002. Am. J. Epidemiol. 181, 127– 136. doi: 10.1093/aje/kwu293 25504027 PMC4351349 · DOI

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Authors
Barcenilla, B. B., Kundel, I., Hall, E., Hilty, N., Ulianich, P., Cook, J., Turley, J., Yerram, M., Min, J.-H., Castillo-González, C., & Shippen, D. E.
Affiliations
Texas A&M University (US)
Corresponding author
Shippen, Dorothy E.
Venue
Frontiers in Plant Science
Published
2024-02-16
Volume
15
Pages
1351613-1351613
ISSN
1664-462X (ISSN-L)
OpenAlex
W4391881534
Cited by
14
References
8
Citations by year
2026: 10 · 2025: 4
FWCI
3.62
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Plant Science (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Aeronautics and Space Administration (80NSSC23K0302)
  • Nuclear Safety and Security Commission
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM065383)
Topics
  • Health Sciences › Medicine › Physiology › Spaceflight effects on biology
  • Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Stress Responses and Tolerance
Keywords
lunar regolith simulant, Arabidopsis thaliana, telomeres, telomere shortening, telomerase activity, oxidative stress, lunar agriculture, antioxidant pretreatment, genome stability

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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