The peculiarities of cell elongation growth of cereal coleoptiles under normal and flooding conditions

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Abstract

The review examines modern knowledge on the mechanisms of the early stages of plant cell elongation growth. Coleoptiles are used as a model object representing juvenile organs of cereal seedlings. Elongation growth is considered to be a protective morphophysiological stage of seedling development during hypogeal germination. The molecular mechanisms of elongation growth include: changes in the properties of the cell wall, activation of proton pumps, as well as aquaporins of plasma membrane and tonoplast. Particular attention is paid to the hormonal system of regulation, including auxin and ethylene. Coleoptiles of rice, a semi-aquatic plant tolerant to oxygen deficiency, demonstrate that the mechanisms of elongation growth are changing intensively under submergence, but they completely ensure cell growth. There is also a redistribution of importance and abundance between phytohormones. The data presented in the review indicate the necessity to continue investigations on the mechanisms of elongation growth under normal and stress conditions.

About the authors

Anastasiia A. Kirpichnikova

Saint Petersburg State University

Email: nastin1972@mail.ru
ORCID iD: 0000-0001-5133-5175
SPIN-code: 9960-9527
Russian Federation, Saint Petersburg

Guzel R. Kudoyarova

Saint Petersburg State University; Ufa Institute of Biology, Ufa Federal Science Center of the Russian Academy of Sciences

Email: guzel@anrb.ru
ORCID iD: 0000-0001-6409-9976
SPIN-code: 6130-3083

Dr. Sci. (Biology), Professor

Russian Federation, Saint Petersburg; Ufa

Vladislav V. Yemelyanov

Saint Petersburg State University

Email: bootika@mail.ru
ORCID iD: 0000-0003-2323-5235
SPIN-code: 9460-1278
http://www.bio.spbu.ru/staff/id179_evv.php

Cand. Sci. (Biology), Assistant Professor

Russian Federation, Saint Petersburg

Maria F. Shishova

Saint Petersburg State University

Author for correspondence.
Email: mshishova@mail.ru
ORCID iD: 0000-0003-3657-2986
SPIN-code: 7842-7611

Dr. Sci. (Bioligy), Professor

Russian Federation, Saint Petersburg

References

  1. Cosgrove DJ. Plant cell wall extensibility: Connecting plant cell growth with cell wall structure, mechanics, and the action of wall-modifying enzymes. J Exp Bot. 2016;67(2):463–476. doi: 10.1093/jxb/erv511
  2. Gorshkova TA. Cell wall is a multifunctional structure of a plant. Los’ DA, editor. LXXX Timiryazev readings. Moscow: Nauka, 2021. 118 p. (In Russ.)
  3. Field BB. The role of auxin in regulatory systems in plants. Chailakhyan MH. XLIV Timiryazev readings. Leningrad: Nauka, 1986. 80 p. (In Russ.)
  4. Hilty J, Muller B, Pantin F, Leuzinger S. Plant growth: The what, the how, and the why. New Phytol. 2021;232(1):25–41. doi: 10.1111/nph.17610
  5. Kutschera U, Deng Z, Oses-Prieto JA, et al. Cessation of coleoptile elongation and loss of auxin sensitivity in developing rye seedlings: A quantitative proteomic analysis. Plant Signal Behav. 2010;5(5):509–517. doi: 10.4161/psb.11210
  6. Inada N, Sakai A, Kuroiwa H, Kuroiwa T. Three-dimensional progression of programmed death in the rice coleoptile. Int Rev Cytol. 2002;218:221–258. doi: 10.1016/s0074-7696(02)18014-4
  7. Zhao X, Niu Y, Hossain Z, et al. New insights into light spectral quality inhibits the plasticity elongation of maize mesocotyl and coleoptile during seed germination. Front Plant Sci. 2023;14:1152399. doi: 10.3389/fpls.2023.1152399
  8. Kawai M, Uchimiya H. Coleoptile senescence in rice (Oryza sativa L.). Ann Bot. 2000;86(2):405–414. doi: 10.1006/anbo.2000.1199
  9. Takahashi H, Saika H, Matsumura H, et al. Cell division and cell elongation in the coleoptile of rice alcohol dehydrogenase 1-deficient mutant are reduced under complete submergence. Ann Bot. 2011;108(2):253–261. doi: 10.1093/aob/mcr137
  10. Edwards JM, Roberts TH, Atwell BJ. Quantifying ATP turnover in anoxic coleoptiles of rice (Oryza sativa) demonstrates preferential allocation of energy to protein synthesis. J Exp Bot. 2012;63(12): 4389–4402. doi: 10.1093/jxb/ers114
  11. O’Sullivan PA, Weiss GM, Friesen D. Tolerance of spring wheat (Triticum aestivum L.) to trifluralin deep-incorporated in the autumn or spring. Weed Res. 1985;25(4):275–280. doi: 10.1111/j.1365-3180.1985.tb00645.x
  12. Brown PR, Singleton GR, Tann CR, Mock I. Increasing sowing depth to reduce mouse damage to winter crops. Crop Prot. 2003;22(4):653–660. doi: 10.1016/S0261-2194(03)00006-1
  13. Rebetzke GJ, Zheng B, Chapman SC. Do wheat breeders have suitable genetic variation to overcome short coleoptiles and poor establishment in the warmer soils of future climates? Funct Plant Biol. 2016;43(10):961–972. doi: 10.1071/FP15362
  14. Atwell BJ, Waters I, Greenway H. The effect of oxygen and turbulence on elongation of coleoptiles of submergence-tolerant and -intolerant rice cultivars. J Exp Bot. 1982;33(5):1030–1044. doi: 10.1093/jxb/33.5.1030
  15. Bogdanova EM, Bertova AD, Kirpichnikova AA, et al. Growth and viability of coleoptiles under oxygen deficiency in Oryza sativa L. FROM the collection of the federal rice research center. Agricultural Biology. 2023;58(3):538–553. doi: 10.15389/agrobiology.2023.3.538rus
  16. Huang S, Shingaki-Wells RN, Petereit J, et al. Temperature-dependent metabolic adaptation of Triticum aestivum seedlings to anoxia. Sci Rep. 2018;8:6151. doi: 10.1038/s41598-018-24419-7
  17. Luo H, Hill CB, Zhou G, et al. Genome-wide association mapping reveals novel genes associated with coleoptile length in a worldwide collection of barley. BMC Plant Biol. 2020;20:346. doi: 10.1186/s12870-020-02547-5
  18. Sharova EI. Cell wall of plants. Saint Petersburg: SPbU Publ., 2004. 156 p. (In Russ.)
  19. Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol. 2005;6(11):850–861. doi: 10.1038/nrm1746
  20. Gorshkova TA. Plant cell wall as a dynamic system. Moscow: Nauka, 2007. 429 p. (In Russ.)
  21. Freshour G, Clay RP, Fuller MS, et al. Developmental and tissue-specific structural alterations of the cell-wall polysaccharides of Arabidopsis thaliana roots. Plant Physiol. 1996;110(4):1413–1429. doi: 10.1104/pp.110.4.1413
  22. Goudenhooft C, Siniscalco D, Arnould O, et al. Investigation of the mechanical properties of flax cell walls during plant development: The relation between performance and cell wall structure. Fibers. 2018;6(1):6. doi: 10.3390/fib6010006
  23. Samalova M, Gahurova E, Hejatko J. Expansin-mediated developmental and adaptive responses: A matter of cell wall biomechanics? Quant Plant Biol. 2022;3: e11. doi: 10.1017/qpb.2022.6
  24. Gibeaut DM, Pauly M, Bacic A, Fincher GB. Changes in cell wall polysaccharides in developing barley (Hordeum vulgare) coleoptiles. Planta. 2005;221:729–738. doi: 10.1007/s00425-005-1481-0
  25. Kozlova LV, Snegireva AV, Gorshkova TA. Distribution and structure of mixed linkage glucan at different stages of elongation of maize root cells. Russ J Plant Physiol. 2012;59(3):339–347. doi: 10.1134/S1021443712030090
  26. Li J, Dickerson TJ, Hoffmann-Benning S. Contribution of proteomics in the identification of novel proteins associated with plant growth. J Proteome Res. 2013;12(11):4882–48891. doi: 10.1021/pr400608d
  27. Niu L, Huang W, Liu L, et al. Differential abundance proteins associated with rapid growth of etiolated coleoptiles in maize. Plant Direct. 2021;5(6):e00332. doi: 10.1002/pld3.332
  28. Long Y, Cheddadi I, Mosca G, et al. Cellular heterogeneity in pressure and growth emerges from tissue topology and geometry. Curr Biol. 2020;30(8):1504–1516.e8. doi: 10.1016/j.cub.2020.02.027
  29. Ali O, Cheddadi I, Landrein B, Long Y. Revisiting the relationship between turgor pressure and plant cell growth. New Phytol. 2023;238(1):62–69. doi: 10.1111/nph.18683
  30. Li Y, Zeng H, Xu F, et al. H+-ATPases in plant growth and stress responses. Annu Rev Plant Biol. 2022;73:495–521. doi: 10.1146/annurev-arplant-102820-114551
  31. Kaiser S, Scheuring D. To lead or to follow: Contribution of the plant vacuole to cell growth. Front Plant Sci. 2020;11:553. doi: 10.3389/fpls.2020.00553
  32. Duckney PJ, Wang P, Hussey PJ. Membrane contact sites and cytoskeleton-membrane interactions in autophagy. FEBS Lett. 2022;596(17):2093–2103. doi: 10.1002/1873-3468.14414
  33. Kaiser S, Eisele S, Scheuring D. Vacuolar occupancy is crucial for cell elongation and growth regardless of the underlying mechanism. Plant Signal Behav. 2021;16(8):e1922796. doi: 10.1080/15592324.2021.1922796
  34. Deamer DW, Bramhall J. Permeability of lipid bilayers to water and ionic solutes. Chem Phys Lipids. 1986;40(2–4):167–188. doi: 10.1016/0009-3084(86)90069-1
  35. Kurowska MM. Aquaporins in cereals — important players in maintaining cell homeostasis under abiotic stress. Genes. 2021;12(4):477. doi: 10.3390/genes12040477
  36. Kudoyarova G, Veselov D, Yemelyanov V, Shishova M. The role of aquaporins in plant growth under conditions of oxygen deficiency. Int J Mol Sci. 2022;23(17):10159. doi: 10.3390/ijms231710159
  37. Martre P, Morillon R, Barrieu F, et al. Plasma membrane aquaporin play a significant role during recovery from water deficit. Plant Physiol. 2002;130(4):2101–2110. doi: 10.1104/pp.009019
  38. Hachez C, Zelazny E, Chaumont F. Modulating the expression of aquaporin genes in planta: A key to understand their physiological functions? Biochim Biophys Acta. 2006;1758(8):1142–1156. doi: 10.1016/j.bbamem.2006.02.017
  39. Wang Y, Zhao Z, Liu F, et al. Versatile roles of aquaporins in plant growth and development. Int J Mol Sci. 2020;21(24):9485. doi: 10.3390/ijms21249485
  40. Moshelion M, Hachez C, Ye Q, et al. Membrane water permeability and aquaporin expression increase during growth of maize suspension cultured cells. Plant Cell Environ. 2009;32(10):1334–1345. doi: 10.1111/j.1365-3040.2009.02001.x
  41. Zhou J-Y, Hao D-L, Yang G-Z. Regulation of cytosolic pH: The contributions of plant plasma membrane H+-ATPases and multiple transporters. Int J Mol Sci. 2021;22(23):12998. doi: 10.3390/ijms222312998
  42. Raghavendra AS, Ye W, Kinoshita T. Editorial: pH as a signal and secondary messenger in plant cells. Front Plant Sci. 2023;14:1148689. doi: 10.3389/fpls.2023.1148689
  43. Barbez E. Root growth: Orchestrating pH levels in plants. eLife. 2023;12:e91025. doi: 10.7554/eLife.91025
  44. Palmgren MG. Plant plasma membrane H+-ATPases: Powerhouses for nutrient uptake. Annu Rev Plant Physiol Plant Mol Biol. 2001;52:817–845. doi: 10.1146/annurev.arplant.52.1.817
  45. Pedersen CN, Axelsen KB, Harper JF, Palmgren MG. Evolution of plant P-type ATPases. Front Plant Sci. 2012;3:31. doi: 10.3389/fpls.2012.00031
  46. Arango M, Gévaudant F, Oufattole M, Boutry M. The plasma membrane proton pump ATPase: the significance of gene subfamilies. Planta. 2003;216(3):355–365. doi: 10.1007/s00425-002-0856-8
  47. Toda Y, Wang Y, Takahashi A, et al. Oryza sativa H+-ATPase (OSA) is involved in the regulation of dumbbell-shaped guard cells of rice. Plant Cell Physiol. 2016;57(6):1220–1230. doi: 10.1093/pcp/pcw070
  48. Falhof J, Pedersen JT, Fuglsang AT, Palmgren M. Plasma membrane H+-ATPase regulation in the center of plant physiology. Mol Plant. 2016;9(3):323–337. doi: 10.1016/j.molp.2015.11.002
  49. Camoni L, Di Lucente C, Pallucca R, et al. Binding of phosphatidic acid to 14-3-3 proteins hampers their ability to activate the plant plasma membrane H+-ATPase. IUBMB Life. 2012;64(8):710–716. doi: 10.1002/iub.1058
  50. Hager A, Debus G, Edel HG, et al. Auxin induces exocytosis and the rapid synthesis of a high-turnover pool of plasma-membrane H+-ATPase. Planta. 1991;185(4):527–537. doi: 10.1007/BF00202963
  51. Rudashevskaya EL, Kirpichnikova AA, Shishova MF. Activity of plasma membrane H+-ATPase in coleoptile cells during development of maize seedlings. Russ J Plant Physiol. 2005;52(4):504–510. doi: 10.1007/s11183-005-0074-x
  52. Rudashevskaya EL, Yakovlev AYu, Yakovleva OV, Shishova MF. Alteration of plasmalemma H+-ATPase activity in maize coleoptile cells at different age of seedlings. Cell Tissue Biol. 2009;3(2):143–148. doi: 10.1134/S1990519X09020059
  53. Shishova MF, Tankelyun OV, Rudashevskaya EL, et al. Alteration of transport activity of proton pumps in coleoptile cells during early development stages of maize seedlings. Russ J Dev Biol. 2012;43(6):342–352. doi: 10.1134/S1062360412060070
  54. Ratajczak R. Structure, function and regulation of the plant vacuolar H(+)-translocating ATPase. Biochim Biophys Acta. 2000;1465(1–2): 17–36. doi: 10.1016/s0005-2736(00)00129-2
  55. Sze H, Schumacher K, Müller ML, et al. A simple nomenclature for a complex proton pump: VHA genes encode the vacuolar H+-ATPase. Trends Plant Sci. 2002;7(4):157–161. doi: 10.1016/s1360-1385(02)02240-9
  56. Kabała K, Janicka M. Structural and functional diversity of two ATP-driven plant proton pumps. Int J Mol Sci. 2023;24(5):4512. doi: 10.3390/ijms24054512
  57. Chen T, Mikhaylova YuV, Shishova MF. Molecular phylogenetic analysis of the tonoplast H+-ATPase subunits. Russ J Genet Appl Res. 2017;7(6):592–606. doi: 10.1134/S207905971706003X
  58. Lupanga U, Rohrich R, Askani J, et al. The Arabidopsis V-ATPase is localized to the TGN/EE via a seed plant-specific motif. eLife. 2020;9:e60568. doi: 10.7554/eLife.60568
  59. Schumacher K, Krebs M. The V-ATPase: Small cargo, large effects. Curr Opin Plant Biol. 2010;13(6):724–730. doi: 10.1016/j.pbi.2010.07.003
  60. Seidel T. The plant V-ATPase. Front Plant Sci. 2022;13:931777. doi: 10.3389/fpls.2022.931777
  61. Klychnikov OI, Li KW, Lill H, de Boer AH. TheV-ATPase from etiolated barley (Hordeum vulgare L.) shoots is activated by blue light and interacts with 14-3-3 proteins. J Exp Bot. 2007;58(5):1013–1023. doi: 10.1093/jxb/erl261
  62. Lüttge U, Fischer-Schliebs E, Ratajczak R. The H+-pumping V-ATPase of higher plants: A versatile eco-enzyme in response to environmental stress. Cell Biol Mol Lett. 2001;6(2A):356–361.
  63. Maeshima M. Vacuolar H(+)-pyrophosphatase. Biochim Biophys Acta. 2000;1465(1–2):37–51. doi: 10.1016/s0005-2736(00)00130-9
  64. Neuhaus HE, Trentmann O. Regulation of transport processes across the tonoplast. Front Plant Sci. 2014;5:460. doi: 10.3389/fpls.2014.00460
  65. Ferjani A, Segami S, Horiguchi G, et al. Keep an eye on PPi: The vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis. Plant Cell. 2011;23(8):2895–2908. doi: 10.1105/tpc.111.085415
  66. Khadilkar AS, Yadav UP, Salazar C, et al. Constitutive and companion cell-specific overexpression of AVP1, encoding a proton-pumping pyrophosphatase, enhances biomass accumulation, phloem loading, and long-distance transport. Plant Physiol. 2016;170(1):401–414. doi: 10.1104/pp.15.01409
  67. Primo C, Pizzio GA, Yang J, et al. Plant proton pumping pyrophosphatase: The potential for its pyrophosphate synthesis activity to modulate plant growth. Plant Biol. 2019;21(6):989–996. doi: 10.1111/plb.13007
  68. Zhang Y, Feng X, Wang L, et al. The structure, functional evolution, and evolutionary trajectories of the H+-PPase gene family in plants. BMC Genom. 2020;21:195. doi: 10.1186/s12864-020-6604-2
  69. Lin S-M, Tsai J-Y, Hsiao C-D, et al. Crystal structure of a membrane-embedded H+-translocating pyrophosphatase. Nature. 2012;484(7394):399–404. doi: 10.1038/nature10963
  70. Hsu Y-D, Huang Y-F, Pan Y-J, et al. Regulation of H+-pyrophosphatase by 14-3-3 Proteins from Arabidopsis thaliana. J Membr Biol. 2018;251(2):263–276. doi: 10.1007/s00232-018-0020-4
  71. Segami S, Asaoka M, Kinoshita S, et al. Biochemical, structural and physiological characteristics of vacuolar H+-pyrophosphatase. Plant Cell Physiol. 2018;59(7):1300–1308. doi: 10.1093/pcp/pcy054
  72. Baroncelli S, Lercari B, Cionini PG, et al. Effect of light and gibberellic acid on coleoptile and first-foliage-leaf growth in durum wheat (Triticum durum Desf.). Planta. 1984;160(4):298–304. doi: 10.1007/BF00393410
  73. Yin C-C, Ma B, Collinge DP, et al. Ethylene responses in rice roots and coleoptiles are differentially regulated by a carotenoid isomerase-mediated abscisic acid pathway. Plant Cell. 2015;27(4):1061–1081. doi: 10.1105/tpc.15.00080
  74. Kutschera U, Wang Z-Y. Growth-limiting proteins in maize coleoptiles and the auxin-brassinosteroid hypothesis of mesocotyl elongation. Protoplasma. 2016;253(1):3–14. doi: 10.1007/s00709-015-0787-4
  75. Rayle DL, Cleland R. Enhancement of wall loosening and elongation by acid solution. Plant Physiol. 1970;46(2):250–253. doi: 10.1104/pp.46.2.250
  76. Nishitani K, Vissenberg K. Roles of the XTH protein family in the expanding cell. In: Verbelen JP, Vissenberg K, editors. The expanding cell. Plant cell monographs. Berlin, Heidelberg, New York: Springer, 2006. Vol. 5. P. 89–116. doi: 10.1007/7089_2006_072
  77. Hocq L, Pelloux J, Lefebvre V. Connecting homogalacturonan-type pectin remodeling to acid growth. Trends Plant Sci. 2017;22(1):20–29. doi: 10.1016/j.tplants.2016.10.009
  78. Cosgrove DJ. Plant expansins: Diversity and interactions with plant cell walls. Curr Opin Plant Biol. 2015;25:162–172. doi: 10.1016/j.pbi.2015.05.014.
  79. McQueen-Mason S, Durachko DM, Cosgrove DJ. Two endogenous proteins that induce cell wall extension in plants. Plant Cell. 1992;4(11):1425–1433. doi: 10.1105/tpc.4.11.1425
  80. Du M, Spalding EP, Gray WM. Rapid auxin-mediated cell expansion. Annu Rev Plant Biol. 2020;71:379–402. doi: 10.1146/annurev-arplant-073019-025907
  81. Dharmasiri N, Dharmasiri S, Estelle M. The F-box protein TIR1 is an auxin receptor. Nature. 2005;435(7041):441–445. doi: 10.1038/nature03543
  82. Dreher KA, Brown J, Saw RE, Callis J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell. 2006;18(3):699–714. doi: 10.1105/tpc.105.039172
  83. Takahashi K, Hayashi K-i, Kinoshita T. Auxin activates the plasma membrane H+-ATPase by phosphorylation during hypocotyl elongation in Arabidopsis. Plant Physiol. 2012;159(2):632–641. doi: 10.1104/pp.112.196428
  84. Stortenbeker N, Bemer M. The SAUR gene family: The plant’s toolbox for adaptation of growth and development. J Exp Bot. 2019;70(1):17–27. doi: 10.1093/jxb/ery332
  85. Lin W, Zhou X, Tang W, et al. TMK-based cell-surface auxin signalling activates cell-wall acidification. Nature. 2021;599(7884): 278–282. doi: 10.1038/s41586-021-03976-4
  86. Kirpichnikova AA, Rudashevskaya EL, Yemelyanov VV, Shishova MF. Ca2+-Transport through plasma membrane as a test of auxin sensitivity. Plants. 2014;3(2):209–222. doi: 10.3390/plants3020209
  87. Fendrych M, Leung J, Friml J. TIR1/AFB-Aux/IAA auxin perception mediates rapid cell wall acidification and growth of Arabidopsis hypocotyls. eLife. 2016;5: e19048. doi: 10.7554/eLife.19048
  88. Xia L, Mar Marquès-Bueno M, Karnik R. Trafficking SNARE SYP132 partakes in auxin-associated root growth. Plant Physiol. 2020;182(4):1836–1840. doi: 10.1104/pp.19.01301
  89. Liu S, Chen H. Ethylene signaling facilitates plant adaption to physical barriers. Front Plant Sci. 2021;12:697988. doi: 10.3389/fpls.2021.697988
  90. Binder BM. Ethylene signaling in plants. J Biol Chem. 2020;295(22):7710–7725. doi: 10.1074/jbc.REV120.010854
  91. Yin C-C, Huang Y-H, Zhang X, et al. Ethylene-mediated regulation of coleoptile elongation in rice seedlings. Plant Cell Environ. 2023;46(4):1060–1074. doi: 10.1111/pce.14492
  92. Wang J-H, Gu K-D, Zhang Q-Y, et al. Ethylene inhibits malate accumulation in apple by transcriptional repression of aluminum-activated malate transporter 9 via the WRKY31-ERF72 network. New Phytol. 2023;239(3):1014–1034. doi: 10.1111/nph.18795
  93. Tungngoen K, Kongsawadworakul P, Viboonjun U, et al. Involvement of HbPIP2;1 and HbTIP1;1 aquaporins in ethylene stimulation of latex yield through regulation of water exchanges between inner liber and latex cells in Hevea brasiliensis. Plant Physiol. 2009;151(2):843–856. doi: 10.1104/pp.109.140228
  94. Karcz W, Kurtyka R. Effect of cadmium on growth, proton extrusion and membrane potential in maize coleoptile segments. Biol Plant. 2007;51(4):713–719. doi: 10.1007/s10535-007-0147-0
  95. González Á, Ayerbe L. Response of coleoptiles to water deficit: Growth, turgor maintenance and osmotic adjustment in barley plants (Hordeum vulgare L.). Agric Sci. 2011;2(3):159–166. doi: 10.4236/as.2011.23022
  96. Nizam I. Effects of salinity stress on water uptake, germination and early seedling growth of perennial ryegrass. Afr J Biotechnol. 2011;10(51):10418–10424. doi: 10.5897/AJB11.1243
  97. Wu Y-S, Yang C-Y. Comprehensive transcriptomic analysis of auxin responses in submerged rice coleoptile growth. Int J Mol Sci. 2020;21(4):1292. doi: 10.3390/ijms21041292
  98. Chirkova T, Yemelyanov V. The study of plant adaptation to oxygen deficiency in Saint Petersburg University. Biol Commun. 2018;63(1):17–31. doi: 10.21638/spbu03.2018.104
  99. Turner FT, Chen C-C, Mccauley GN. Morphological development of rice seedlings in water at controlled oxygen levels. Agron J. 1981;73(3):566–568. doi: 10.2134/agronj1981.00021962007300030037x
  100. Ismail AM, Ella ES, Vergara GV. Mechanisms associated with tolerance to submergence during germination and early seedling growth in rice (Oryza sativa). Ann Bot. 2009;103(2):197–209. doi: 10.1093/aob/mcn211
  101. Su X, Wu H, Xiang J, et al. Evaluation of submergence tolerance of different rice genotypes at seedling emergence stage under water direct seeding. OALib J. 2022;9: e8706. doi: 10.4236/oalib.1108706
  102. Kordan HA. Patterns of shoot and root growth in rice seedlings germinating under water. J Appl Ecol. 1974;11(2):685–690. doi: 10.2307/2402218
  103. Shiono K, Koshide A, Iwasaki K, et al. Imaging the snorkel effect during submerged germination in rice: Oxygen supply via the coleoptile triggers seminal root emergence underwater. Front Plant Sci. 2022;13:946776. doi: 10.3389/fpls.2022.946776
  104. Narsai R, Edwards JM, Roberts TH, et al. Mechanisms of growth and patterns of gene expression in oxygen-deprived rice coleoptiles. Plant J. 2015;82(1):25–40. doi: 10.1111/tpj.12786
  105. Hsu S-K, Tung C-W. RNA-Seq analysis of diverse rice genotypes to identify the genes controlling coleoptile growth during submerged germination. Front Plant Sci. 2017;8:762. doi: 10.3389/fpls.2017.00762
  106. Lasanthi-Kudahettige R, Magneschi L, Loreti E, et al. Transcript profiling of the anoxic rice coleoptile. Plant Physiol. 2007;144(1): 218–231. doi: 10.1104/pp.106.093997
  107. Magneschi L, Lasanthi-Kudahettige R, Alpi A, Perata P. Expansin gene expression and anoxic coleoptile elongation in rice cultivars. J Plant Physiol. 2009;166(14):1576–1580. doi: 10.1016/j.jplph.2009.03.008
  108. Lee T-M, Lin Y-H. Peroxidase activity in relation to ethylene-induced rice (Oryza sativa L.) coleoptile elongation. Bot Bull Acad Sin. 1996;37(4):239–245.
  109. Ishizawa K, Esashi Y. Gaseous factors involved in the enhanced elongation of rice coleoptiles under water. Plant Cell Environ. 1984;7(4):239–245. doi: 10.1111/1365-3040.ep11589438
  110. Hager A. Avena coleoptile segments: Hyperelongation growth after anaerobic treatment. Z Naturforsch C. 1980;35(9):794–804. doi: 10.1515/znc-1980-9-1022
  111. Yemelyanov VV, Chirkova TV, Lindberg SM, Shishova MF. Potassium efflux and cytosol acidification as primary anoxia-induced events in wheat and rice seedlings. Plants. 2020;9(9):1216. doi: 10.3390/plants9091216
  112. Baykov AA, Malinen AM, Luoto HH, Lahti R. Pyrophosphate-fueled Na+ and H+ transport in prokaryotes. Microbiol Mol Biol Rev. 2013;77(2):267–276. doi: 10.1128/MMBR.00003-13
  113. Carystinos GD, MacDonald HR, Monroy AF, et al. Vacuolar H(+)-translocating pyrophosphatase is induced by anoxia or chilling in seedlings of rice. Plant Physiol. 1995;108(2):641–649. doi: 10.1104/pp.108.2.641
  114. Mohanty B. Promoter architecture and transcriptional regulation of genes upregulated in germination and coleoptile elongation of diverse rice genotypes tolerant to submergence. Front Genet. 2021;12:639654. doi: 10.3389/fgene.2021.639654
  115. Pegoraro R, Mapelli S, Torti G, Bertani A. Indole-3-acetic acid and rice coleoptile elongation under anoxia. J Plant Growth Regul. 1988;7:85–94. doi: 10.1007/BF02025378
  116. Horton RF. The effect of ethylene and other regulators on coleoptile growth of rice under anoxia. Plant Sci. 1991;79(1):57–62. doi: 10.1016/0168-9452(91)90069-K
  117. Nghi KN, Tondelli A, Vale G, et al. Dissection of coleoptile elongation in japonica rice under submergence through integrated genome-wide association mapping and transcriptional analyses. Plant Cell Environ. 2019;42(6):1832–1846. doi: 10.1111/pce.13540
  118. Nghi KN, Tagliani A, Mariotti L, et al. Auxin is required for the long coleoptile trait in japonica rice under submergence. New Phytol. 2021;229(1):85–93. doi: 10.1111/nph.16781
  119. Bailey-Serres J, Fukao T, Gibbs DJ, et al. Making sense of low oxygen sensing. Trends Plant Sci. 2012;17(3):129–138. doi: 10.1016/j.tplants.2011.12.004

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