Stele tissues of chickpea roots show higher metabolic activity than the cortex, independent of external O2 supply
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
NNF23OC0084801
Novo Nordisk Fonden
CV23-0039
Carlsbergfondet
101061962
European Union
19-03-KU
Danida Fellowship Centre
25-07-KU
Danida Fellowship Centre
LO1415
Ministry of Education, Youth and SportsKarmelitska 529/5118 12 Prague 1 Czech Republic
PubMed
41239768
DOI
10.1111/nph.70737
Knihovny.cz E-zdroje
- Klíčová slova
- Cicer arietinum, O2 diffusion, anaerobic metabolism, anoxic cores, bulky tissues, respiration, stele hypoxia,
- MeSH
- antioxidancia metabolismus MeSH
- Cicer * metabolismus enzymologie účinky léků MeSH
- kořeny rostlin * metabolismus enzymologie účinky léků cytologie MeSH
- kyslík * metabolismus farmakologie MeSH
- metabolismus sacharidů MeSH
- parciální tlak MeSH
- spotřeba kyslíku MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antioxidancia MeSH
- kyslík * MeSH
Variations in external O2 supply, tissue diffusivity, and O2 consumption rates determine internal O2 gradients in roots. We tested the hypothesis that root metabolism differs between cortex and stele tissues in response to external partial pressure of O2 (pO2). Using O2 microsensors, we measured in vivo O2 dynamics in Cicer arietinum, chickpea, primary roots of contrasting diameters exposed to different external pO2 levels. Respiratory O2 consumption was assessed in the isolated cortex (plus epidermis) and stele tissues. Additionally, activity profiles for 23 key enzymes of carbohydrate and antioxidant metabolism were determined under aerobic, hypoxic, and severely hypoxic conditions. The stele of thick roots (1900 μm) became severely hypoxic/anoxic (≤ 0.3 kPa) even under external air equilibrium, whereas thinner roots (900 μm) remained oxic-to-hypoxic (c. 11.9 kPa). The stele had a 3.3-fold higher O2 consumption rate than the cortex. In 1400 μm roots, severe hypoxia occurred in the stele at 8.9 kPa external pO2 and in the cortex at 4.5 kPa. Activities of carbohydrates and antioxidant enzymes were consistently higher in the stele than in the cortex, regardless of external pO2, indicating that tissue type, in addition to external O2 availability, plays a key role in determining root metabolic activity.
Department of Biology University of Copenhagen 2100 Copenhagen Denmark
Department of Plant and Environmental Sciences University of Copenhagen 2630 Taastrup Denmark
Global Change Research Institute of the Czech Academy of Sciences 603 00 Brno Czech Republic
School of Biological Sciences The University of Western Australia Nedlands WA 6009 Australia
UWA Institute of Agriculture The University of Western Australia Nedlands WA 6009 Australia
Zobrazit více v PubMed
Aguilar EA, Turner DW, Gibbs DJ, Armstrong W, Sivasithamparam K. 2003. Oxygen distribution and movement, respiration and nutrient loading in banana roots (Musa spp. L.) subjected to aerated and oxygen‐depleted environments. Plant and Soil 253: 91–102.
Albrecht G, Mustroph A. 2003. Sucrose utilization via invertase and sucrose synthase with respect to accumulation of cellulose and callose synthesis in wheat roots under oxygen deficiency. Russian Journal of Plant Physiology 50: 813–820.
Armstrong W. 1979. Aeration in higher plants. In: Woolhouse HW, ed. Advances in botanical research. London, UK: Academic Press, 225–332.
Armstrong W, Beckett PM. 1985. Root aeration in unsaturated soil: a multi‐shelled mathematical model of oxygen diffusion and distribution with and without sectoral wet‐soil blocking of the diffusion path. New Phytologist 100: 293–311.
Armstrong W, Beckett PM, Colmer TD, Setter TL, Greenway H. 2019. Tolerance of roots to low oxygen: ‘anoxic’ cores, the phytoglobin‐nitric oxide cycle, and energy or oxygen sensing. Journal of Plant Physiology 239: 92–108.
Armstrong W, Healy MT, Webb T. 1982. Oxygen diffusion in pea. New Phytologist 91: 647–659.
Armstrong W, Webb T, Darwent M, Beckett PM. 2009. Measuring and interpreting respiratory critical oxygen pressures in roots. Annals of Botany 103: 281–293.
Bieniawska Z, Paul Barratt DH, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM. 2007. Analysis of the sucrose synthase gene family in Arabidopsis. The Plant Journal 49: 810–828.
Cleland RE, Fujiwara T, Lucas WJ. 1994. Plasmodesmal‐mediated cell‐to‐cell transport in wheat roots is modulated by anaerobic stress. Protoplasma 178: 81–85.
Colmer TD, Greenway H. 2011. Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62: 39–57.
Colmer TD, Kotula L, Malik AI, Takahashi H, Konnerup D, Nakazono M, Pedersen O. 2019. Rice acclimation to soil flooding: low concentrations of organic acids can trigger a barrier to radial oxygen loss in roots. Plant, Cell & Environment 42: 2183–2197.
Colmer TD, Winkel A, Kotula L, Armstrong W, Revsbech NP, Pedersen O. 2020. Root O2 consumption, CO2 production and tissue concentration profiles in chickpea, as influenced by environmental hypoxia. New Phytologist 226: 373–384.
Darwent MJ, Armstrong W, Armstrong J, Beckett PM. 2003. Exploring the radial and longitudinal aeration of primary maize roots by means of clark‐type oxygen microelectrodes. Russian Journal of Plant Physiology 50: 722–732.
Fimognari L, Dölker R, Kaselyte G, Jensen CNG, Akhtar SS, Großkinsky DK, Roitsch T. 2020. Simple semi‐high throughput determination of activity signatures of key antioxidant enzymes for physiological phenotyping. Plant Methods 16: 42.
Gibbs J, Bruxelle G, Armstrong W, Greenway H. 1995. Evidence for anoxic zones in 2‐3 mm tips of aerenchymatous maize roots under low O2 supply. Functional Plant Biology 22: 723–730.
Gibbs J, Greenway H. 2003. Mechanisms of anoxia tolerance in plants. I. Growth, survival and anaerobic catabolism. Functional Plant Biology 30: 353.
Gibbs J, Turner DW, Armstrong W, Darwent MJ, Greenway H. 1998. Response to oxygen deficiency in primary maize roots. I. Development of oxygen deficiency in the stele reduces radial solute transport to the xylem. Functional Plant Biology 25: 745–758.
Igamberdiev AU, Baron K, Manac'h‐Little N, Stoimenova M, Hill RD. 2005. The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signalling. Annals of Botany 96: 557–564.
Jammer A, Akhtar SS, Amby DB, Pandey C, Mekureyaw MF, Bak F, Roth PM, Roitsch T. 2022. Enzyme activity profiling for physiological phenotyping within functional phenomics: plant growth and stress responses. Journal of Experimental Botany 73: 5170–5198.
Jammer A, Albacete A, Schulz B, Koch W, Weltmeier F, van der Graaff E, Pfeifhofer HW, Roitsch TG. 2020. Early‐stage sugar beet taproot development is characterized by three distinct physiological phases. Plant Direct 4: e00221.
Jiménez JC, Armstrong W, Colmer TD, Pedersen O. 2024a. Overcoming constraints to measuring O2 diffusivity and consumption of intact roots. Plant Physiology 195: 283–286.
Jiménez JC, Noorrohmah S, Suresh K, Zeisler‐Diehl VV, Peralta Ogorek LL, Herzog M, Pellegrini E, Nagai K, Ashikari M, Takahashi H et al. 2024b. Leaf gas film 1 promotes glycerol ester accumulation and formation of a tight root barrier to radial O2 loss in rice. Plant Physiology 196: 2437–2449.
Justin SHFW, Armstrong W. 1987. The anatomical characteristics of roots and plant responses to soil flooding. New Phytologist 106: 465–495.
Khan HA, Siddique KHM, Colmer TD. 2016. Vegetative and reproductive growth of salt‐stressed chickpea are carbon‐limited: sucrose infusion at the reproductive stage improves salt tolerance. Journal of Experimental Botany 68: 2001–2011.
Kotula L, Clode PL, Jiménez JC, Colmer TD. 2019. Salinity tolerance in chickpea is associated with the ability to ‘exclude’ Na from leaf mesophyll cells. Journal of Experimental Botany 70: 4991–5002.
Kotula L, Clode PL, Striker GG, Pedersen O, Lauchli A, Shabala S, Colmer TD. 2015. Oxygen deficiency and salinity affect cell‐specific ion concentrations in adventitious roots of barley (Hordeum vulgare). New Phytologist 208: 1114–1125.
Laan P, Tosserams M, Blom CWPM, Veen BW. 1990. Internal oxygen transport in Rumex species and its significance for respiration under hypoxic conditions. Plant and Soil 122: 39–46.
Lu Wong W‐J, Ap Rees T. 1971. Carbohydrate oxidation in stele and cortex isolated from roots of Pisum sativum. Biochimica et Biophysica Acta (BBA) – General Subjects 252: 296–304.
McDonald MP, Galwey NW, Colmer TD. 2002. Similarity and diversity in adventitious root anatomy as related to root aeration among a range of wetland and dryland grass species. Plant, Cell & Environment 25: 441–451.
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7: 405–410.
Pandey C, Großkinsky DK, Westergaard JC, Jørgensen HJL, Svensgaard J, Christensen S, Schulz A, Roitsch T. 2021. Identification of a bio‐signature for barley resistance against Pyrenophora teres infection based on physiological, molecular and sensor‐based phenotyping. Plant Science 313: 111072.
Pang J, Shabala S. 2010. Membrane transporters and waterlogging tolerance. In: Mancuso S, Shabala S, eds. Waterlogging signalling and tolerance in plants. Berlin, Heidelberg, Germany: Springer, 197–219.
Pathuri IP, Reitberger IE, Hückelhoven R, Proels RK. 2011. Alcohol dehydrogenase 1 of barley modulates susceptibility to the parasitic fungus Blumeria graminis f.sp. hordei. Journal of Experimental Botany 62: 3449–3457.
Pedersen O, Nakayama Y, Yasue H, Kurokawa Y, Takahashi H, Heidi Floytrup A, Omori F, Mano Y, David Colmer T, Nakazono M. 2021. Lateral roots, in addition to adventitious roots, form a barrier to radial oxygen loss in Zea nicaraguensis and a chromosome segment introgression line in maize. New Phytologist 229: 94–105.
Peralta Ogorek LL, Jiménez JC, Visser EJW, Takahashi H, Nakazono M, Shabala S, Pedersen O. 2024. Outer apoplastic barriers in roots: prospects for abiotic stress tolerance. Functional Plant Biology 51: FP23133.
R Core Team. 2025. R: a language environment for statistical computing. R Foundation for Statistical Computing. [WWW document] URL https://www.R-project.org/
Rolletschek H, Borisjuk L, Gómez‐Álvarez EM, Pucciariello C. 2025. Advances in seed hypoxia research. Plant Physiology 197: kiae556.
Saleem M, Lamkemeyer T, Schützenmeister A, Madlung J, Sakai H, Piepho H‐P, Nordheim A, Hochholdinger F. 2009. Specification of cortical parenchyma and stele of maize primary roots by asymmetric levels of auxin, cytokinin, and cytokinin‐regulated proteins plant physiology. Plant Physiology 152: 4–18.
Shabala S, Shabala L, Barcelo J, Poschenrieder C. 2014. Membrane transporters mediating root signalling and adaptive responses to oxygen deprivation and soil flooding. Plant, Cell & Environment 37: 2216–2233.
Silva‐Cardenas RI, Ricard B, Saglio P, Hill RD. 2003. Hemoglobin and hypoxic acclimation in maize root tips. Russian Journal of Plant Physiology 50: 821–826.
Thomson CJ, Greenway H. 1991. Metabolic evidence for stelar anoxia in maize roots exposed to low O2 concentrations. Plant Physiology 96: 1294–1301.
Trevaskis B, Watts RA, Andersson CR, Llewellyn DJ, Hargrove MS, Olson JS, Dennis ES, Peacock WJ. 1997. Two hemoglobin genes in Arabidopsis thaliana: the evolutionary origins of leghemoglobins. Proceedings of the National Academy of Sciences, USA 94: 12230–12234.
Ward JM, Kühn C, Tegeder M, Frommer WB. 1997. Sucrose transport in higher plants. In: Jeon KW, ed. International review of cytology. Amsterdam, the Netherlands: Academic Press, 41–71.
Zeleneva IV, Savost'yanova EV, Khavkin ÉE. 1982. Enzyme distribution of the cortex and the stele in cytodifferentiating maize seedlings. Biochemie und Physiologie der Pflanzen 177: 97–106.
Zeng Y, Wu Y, Avigne WT, Koch KE. 1998. Differential regulation of sugar‐sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses. Plant Physiology 116: 1573–1583.
Zeng Y, Wu Y, Avigne WT, Koch KE. 1999. Rapid repression of maize invertases by low oxygen. Invertase/sucrose synthase balance, sugar signaling potential, and seedling survival. Plant Physiology 121: 599–608.