Cartwheel aerenchyma in Cardamine amara as a model of schizogenous tissue formation in plants
Status PubMed-not-MEDLINE Language English Country United States Media electronic-ecollection
Document type Journal Article
PubMed
40761292
PubMed Central
PMC12320073
DOI
10.1016/j.isci.2025.113106
PII: S2589-0042(25)01367-7
Knihovny.cz E-resources
- Keywords
- Plant anatomy, Plant biology, Plant development, Plant physiology,
- Publication type
- Journal Article MeSH
Root aerenchyma is essential for survival under waterlogged conditions for plants. It has been necessary to explore a model system of schizogenous aerenchyma in Brassicaceae. Here, we report the formation of schizogenous aerenchyma in primary roots of seedlings of Cardamine amara showing a rather simple cartwheel pattern. The formation of the aerenchyma was suggested to involve three developmental processes: (1) formation of a three-layered cortex, (2) circumferential division of the outer layer of the cortex, and (3) circumferential detachment of cells in the middle layer of the cortex. The root aerenchyma of the C. amara seedling discovered here is the simplest one ever reported, and is a suitable candidate for the model of schizogenous aerenchyma development in plants.
Center for Ecological Research Kyoto University Otsu 520 2113 Japan
Department of Biology Graduate School of Science Kobe University Kobe 657 8501 Japan
Department of Botany Faculty of Science Charles University 128 01 Praha Czech Republic
Kihara Institute for Biological Research Yokohama City University Yokohama 244 0813 Japan
See more in PubMed
Evans D.E. Aerenchyma formation. New Phytol. 2003;161:35–49. doi: 10.1046/j.1469-8137.2003.00907.x. DOI
Seago J.L., Marsh L.C., Stevens K.J., Soukup A., Votrubová O., Enstone D.E. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma. Ann. Bot. 2005;96:565–579. doi: 10.1093/aob/mci211. PubMed DOI PMC
Arber A. Cambridge University Press; 1920. Water Plants, a Study of Aquatic Angiosperms. DOI
Jung J., Lee S.C., Choi H.-K. Anatomical patterns of aerenchyma in aquatic and wetland plants. J. Plant Biol. 2008;51:428–439. doi: 10.1007/BF03036065. DOI
Joshi R., Kumar P. Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots. Physiol. Mol. Biol. Plants. 2012;18:1–9. doi: 10.1007/s12298-011-0093-3. PubMed DOI PMC
Takahashi H., Yamauchi T., Colmer T.D., Nakazono M. In: van Dongen J.T., Licausi F., editors. Vol. 21. Springer-Verlag; Wien: 2014. Aerenchyma formation in plants; pp. 247–265. (Low-Oxygen Stress in Plants, Plant Cell Monographs).
Yamauchi T., Tanaka A., Inahashi H., Nishizawa N.K., Tsutsumi N., Inukai Y., Nakazono M. Fine control of aerenchyma and lateral root development through AUX/IAA- and ARF-dependent auxin signaling. Proc Natl Acad Sci USA. 2019;116:20770–20775. doi: 10.1073/pnas.1907181116. PubMed DOI PMC
Yamauchi T., Nakazono M. Mechanisms of lysigenous aerenchyma formation under abiotic stress. Trends Plant Sci. 2022;27:13–15. doi: 10.1016/j.tplants.2021.10.012. PubMed DOI
Ishizaki K. Development of schizogenous intercellular spaces in plants. Front. Plant Sci. 2015;6:497. doi: 10.3389/fpls.2015.00497. PubMed DOI PMC
Dolan L., Janmaat K., Willemsen V., Linstead P., Poethig S., Roberts K., Scheres B. Cellular organisation of the Arabidopsis thaliana root. Development. 1993;119:71–84. doi: 10.1242/dev.119.1.71. PubMed DOI
Petricka J.J., Winter C.M., Benfey P.N. Control of Arabidopsis root development. Annu. Rev. Plant Biol. 2012;63:563–590. doi: 10.1146/annurev-arplant-042811-105501. PubMed DOI PMC
Mühlenbock P., Plaszczyca M., Plaszczyca M., Mellerowicz E., Karpinski S. Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. Plant Cell. 2007;19:3819–3830. doi: 10.1105/tpc.106.048843. PubMed DOI PMC
Combs-Giroir R., Gschwend A.R. Physical and molecular responses to flooding in Brassicaceae. Environ. Exp. Bot. 2024;219 doi: 10.1016/j.envexpbot.2024.105664. DOI
Nowak J.S., Ono J., Cronk Q.C.B. Anatomical study of an aquatic mustard: Subularia aquatica (Brassicaceae) Aquat. Bot. 2010;93:55–58. doi: 10.1016/j.aquabot.2010.02.004. DOI
Xiang J., Ming J., Yin H., Zhu Y., Li Y., Long L., Ye Z., Wang H., Wang X., Zhang F., et al. Anatomy and histochemistry of the roots and shoots in the aquatic selenium hyperaccumulator Cardamine hupingshanensis (Brassicaceae) Open Life Sci. 2019;14:318–326. doi: 10.1515/biol-2019-0035. PubMed DOI PMC
Lihová J., Marhold K. In: Sharma A.K., Sharma A., editors. 1C. Science Publishers; 2006. Phylogenetic and diversity patterns in Cardamine (Brassicaceae)––a genus with conspicuous polyploid and reticulate evolution; pp. 149–186. (Genome: Biodiversity and Evolution. Phanerogams (Angiosperms–Dicotyledons) Plant).
Marhold K., Kempa M., Kučera J., Skokanová K., Smatanová J., Šingliarová B., Šlenker M., Zozomová-Lihová J. Database of names, chromosome numbers, ploidy levels and genome sizes of the tribe Cardamineae. 2021+. https://cardamine.sav.sk
Yatsu Y., Kachi N., Kudoh H. Ecological distribution and phenology of an invasive species, Cardamine hirsuta L., and its native counterpart, Cardamine flexuosa With., in central Japan. Plant Species Biol. 2003;18:35–42. doi: 10.1046/j.1442-1984.2003.00086.x. DOI
Shimizu-Inatsugi R., Terada A., Hirose K., Kudoh H., Sese J., Shimizu K.K. Plant adaptive radiation mediated by polyploid plasticity in transcriptomes. Mol. Ecol. 2017;26:193–207. doi: 10.1111/mec.13738. PubMed DOI
Mandáková T., Zozomová-Lihová J., Kudoh H., Zhao Y., Lysak M.A., Marhold K. The story of promiscuous crucifers: origin and genome evolution of an invasive species, Cardamine occulta (Brassicaceae), and its relatives. Ann. Bot. 2019;124:209–220. doi: 10.1093/aob/mcz019. PubMed DOI PMC
Soga E., Sugisaka J., Watanabe M., Kudoh H. Population differentiation in the leaf shape and growth form of Cardamine scutata Thunb. in tidal and non-tidal habitats. Plant Species Biol. 2021;36:399–411. doi: 10.1111/1442-1984.12325. DOI
Akiyama R., Sun J., Hatakeyama M., Lischer H.E.L., Briskine R.V., Hay A., Gan X., Tsiantis M., Kudoh H., Kanaoka M.M., et al. Fine-scale empirical data on niche divergence and homeolog expression patterns in an allopolyploid and its diploid progenitor species. New Phytol. 2021;229:3587–3601. doi: 10.1111/nph.17101. PubMed DOI PMC
Johnston J.S., Pepper A.E., Hall A.E., Chen Z.J., Hodnett G., Drabek J., Lopez R., Price H.J. Evolution of genome size in Brassicaceae. Ann. Bot. 2005;95:229–235. doi: 10.1093/aob/mci016. PubMed DOI PMC
Cederholm H.M., Iyer-Pascuzzi A.S., Benfey P.N. Patterning the primary root in Arabidopsis. WIREs Dev. Biol. 2012;1:675–691. doi: 10.1002/wdev.49. PubMed DOI
Helariutta Y., Fukaki H., Wysocka-Diller J., Nakajima K., Jung J., Sena G., Hauser M.-T., Benfey P.N. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell. 2000;101:555–567. doi: 10.1016/S0092-8674(00)80865-X. PubMed DOI
Winter C.M., Szekely P., Popov V., Belcher H., Carter R., Jones M., Fraser S.E., Truong T.V., Benfey P.N. SHR and SCR coordinate root patterning and growth early in the cell cycle. Nature. 2024;626:611–616. doi: 10.1038/s41586-023-06971-z. PubMed DOI PMC
Marhold K. Taxonomy of the genus Cardamine L. (Cruciferae) in the Carpathians and Pannonia. II.Cardamine amara L. Folia Geobot. 1995;30:63–80. doi: 10.1007/BF02813221. DOI
Koch M., Huthmann M., Bernhardt K.-G. Cardamine amara L. (Brassicaceae) in dynamic habitats: Genetic composition and diversity of seed bank and established populations. Basic Appl. Ecol. 2003;4:339–348. doi: 10.1078/1439-1791-00165. DOI
Hay A.S., Pieper B., Cooke E., Mandáková T., Cartolano M., Tattersall A.D., Ioio R.D., McGowan S.J., Barkoulas M., Galinha C., et al. Cardamine hirsuta: a versatile genetic system for comparative studies. Plant J. 2014;78:1–15. doi: 10.1111/tpj.12447. PubMed DOI
Kurihara D., Mizuta Y., Nagahara S., Higashiyama T. ClearSeeAlpha: advanced optical clearing for whole-plant imaging. Plant Cell Physiol. 2021;62:1302–1310. doi: 10.1093/pcp/pcab033. PubMed DOI PMC
Shiono K., Ogawa S., Yamazaki S., Isoda H., Fujimura T., Nakazono M., Colmer T.D. Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths. Ann. Bot. 2011;107:89–99. doi: 10.1093/aob/mcq221. PubMed DOI PMC