Prolonged exposure to hypergravity increases number and size of cells and enhances lignin deposition in the stem of Arabidopsis thaliana.
Arabidopsis thaliana
Gravitational acceleration
Gravity resistance response
Hypergravity
Lignin deposition
Quantitative morphological analysis
Journal
Journal of plant research
ISSN: 1618-0860
Titre abrégé: J Plant Res
Pays: Japan
ID NLM: 9887853
Informations de publication
Date de publication:
02 Jul 2024
02 Jul 2024
Historique:
received:
25
12
2023
accepted:
10
06
2024
medline:
2
7
2024
pubmed:
2
7
2024
entrez:
2
7
2024
Statut:
aheadofprint
Résumé
We have performed a lab-based hypergravity cultivation experiment using a centrifuge equipped with a lighting system and examined long-term effects of hypergravity on the development of the main axis of the Arabidopsis (Arabidopsis thaliana (L.) Heynh.) primary inflorescence, which comprises the rachis and peduncle, collectively referred to as the main stem for simplicity. Plants grown under 1 × g (gravitational acceleration on Earth) conditions for 20-23 days and having the first visible flower bud were exposed to hypergravity at 8 × g for 10 days. We analyzed the effect of prolonged hypergravity conditions on growth, lignin deposition, and tissue anatomy of the main stem. As a result, the length of the main stem decreased and cross-sectional area, dry mass per unit length, cell number, and lignin content of the main stem significantly increased under hypergravity. Lignin content in the rosette leaves also increased when they were exposed to hypergravity during their development. Except for interfascicular fibers, cross-sectional areas of the tissues composing the internode significantly increased under hypergravity in most types of the tissues in the basal part than the apical part of the main stem, indicating that the effect of hypergravity is more pronounced in the basal part than the apical part. The number of cells in the fascicular cambium and xylem significantly increased under hypergravity both in the apical and basal internodes of the main stem, indicating a possibility that hypergravity stimulates procambium activity to produce xylem element more than phloem element. The main stem was suggested to be strengthened through changes in its morphological characteristics as well as lignin deposition under prolonged hypergravity conditions.
Identifiants
pubmed: 38954119
doi: 10.1007/s10265-024-01556-x
pii: 10.1007/s10265-024-01556-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Japan Society for the Promotion of Science
ID : 21570064
Organisme : Japan Society for the Promotion of Science
ID : 24620003
Organisme : Japan Society for the Promotion of Science
ID : 15K11914
Organisme : Institute of Space and Astronautical Science
ID : 2022 Front loading research grant
Informations de copyright
© 2024. The Author(s) under exclusive licence to The Botanical Society of Japan.
Références
Allen J, Bisbee PA, Darnell RL, Kuang A, Levine LH, Musgrave ME, van Loon JJWA (2009) Gravity control of growth form in Brassica rapa and Arabidopsis thaliana (Brassicaceae): consequences for secondary metabolism. Am J Bot 96:652–660
doi: 10.3732/ajb.0800261
pubmed: 21628221
Boyes DC, Zayed AM, Ascenzi R, McCaskill AJ, Hoffman NE, Davis KR (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510
pubmed: 11449047
pmcid: 139543
De Jaegher G, Boyer N, Gaspar T (1985) Thigmomorphogenesis inBryonia Dioica: changes in soluble and wall peroxidases, phenylalanine ammonia-lyase activity, cellulose, lignin content and monomeric constituents. Plant Growth Regul 3:133–148
doi: 10.1007/BF01806053
Fitzelle KJ, Kiss JZ (2001) Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. J Exp Bot 52:265–275
doi: 10.1093/jexbot/52.355.265
pubmed: 11283171
Hattori T, Otomi Y, Nakajima Y, Soga K, Wakabayashi K, Iida H, Hoson T (2020) MCA1 and MCA2 are involved in the response to hypergravity in Arabidopsis hypocotyls. Plants 9:590
doi: 10.3390/plants9050590
pubmed: 32380659
pmcid: 7285502
Hosamani R, Swamy BK, Dsouza A, Sathasivam M (2022) Plant responses to hypergravity: a comprehensive review. Planta 257:17
doi: 10.1007/s00425-022-04051-6
pubmed: 36534189
Hoson T, Soga K (2003) New aspects of gravity responses in plant cells. Int Rev Cytol 229:209–244
doi: 10.1016/S0074-7696(03)29005-7
pubmed: 14669957
Karahara I, Suto T, Yamaguchi T, Yashiro U, Tamaoki D, Okamoto E, Yano S, Tanigaki F, Shimazu T, Kasahara H, Kasahara H, Yamada M, Hoson T, Soga K, Kamisaka S (2020) Vegetative and reproductive growth of Arabidopsis under microgravity conditions in space. J Plant Res 133:571–585
doi: 10.1007/s10265-020-01200-4
pubmed: 32424466
Link BM, Durst SJ, Zhou W, Stankovic B (2003) Seed-to-seed growth of Arabidopsis thaliana on the International Space Station. Adv Space Res 31:2237–2243
doi: 10.1016/S0273-1177(03)00250-3
pubmed: 14686438
Link BM, Busse J, Stankovic B (2014) Seed-to-seed-to-seed growth and development of Arabidopsis in microgravity. Astrobiology 14:866–875
doi: 10.1089/ast.2014.1184
pubmed: 25317938
pmcid: 4201294
Merkys AI, Laurinavicius RS (1983) Complete cycle of individual development of Arabidopsis thaliana (L.) Heynh. Plants on board the Salyut-7 orbital station. Dokl Akad Nauk SSSR 271:579–512
Morrison IM (1972) A semi-micro method for the determination of lignin and its use in predicting the digestibility of forage crops. J Sci Food Agric 23:455–463
doi: 10.1002/jsfa.2740230405
pubmed: 5029974
Musgrave ME, Kuang A (2003) Plant reproductive development during spaceflight. In: Hans-Jurg M (ed) Adv Space Biol Med, vol 9. Elsevier, pp 1–23
Musgrave ME, Kuang A, Xiao Y, Stout SC, Bingham GE, Briarty LG, Levenskikh MA, Sychev VN, Podolski IG (2000) Gravity independence of seed-to-seed cycling in Brassica rapa. Planta 210:400–406
doi: 10.1007/PL00008148
pubmed: 10750897
Musgrave ME, Kuang A, Tuominen LK, Levine LH, Morrow RC (2005) Seed storage reserves and glucosinolates in Brassica rapa L. grown on the International Space Station. J Am Soc Hortic Sci 130:848–856
doi: 10.21273/JASHS.130.6.848
Nakabayashi I, Karahara I, Tamaoki D, Masuda K, Wakasugi T, Yamada K, Soga K, Hoson T, Kamisaka S (2006) Hypergravity stimulus enhances primary xylem development and decreases mechanical properties of secondary cell walls in inflorescence stems of Arabidopsis thaliana. Ann Bot (Lond) 97:1083–1090
doi: 10.1093/aob/mcl055
Nakano M, Furuichi T, Sokabe M, Iida H, Tatsumi H (2021) The gravistimulation-induced very slow Ca2 + increase in Arabidopsis seedlings requires MCA1, a Ca2+-permeable mechanosensitive channel. Sci Rep 11:227
doi: 10.1038/s41598-020-80733-z
pubmed: 33420331
pmcid: 7794229
Ohashi-Ito K, Fukuda H (2010) Transcriptional regulation of vascular cell fates. Curr Opin Plant Biol 13:670–676
doi: 10.1016/j.pbi.2010.08.011
pubmed: 20869293
Soga K (2013) Resistance of plants to gravitational force. J Plant Res 126:589–596
doi: 10.1007/s10265-013-0572-4
pubmed: 23732635
Soga K, Wakabayashi K, Kamisaka S, Hoson T (2005) Hypergravity inhibits elongation growth of azuki bean epicotyls independently of the direction of stimuli. Adv Space Res 36:1269–1276
doi: 10.1016/j.asr.2005.05.029
Stutte GW, Monje O, Hatfield RD, Paul AL, Ferl RJ, Simone CG (2006) Microgravity effects on leaf morphology, cell structure, carbon metabolism and mRNA expression of dwarf wheat. Planta 224:1038–1049
doi: 10.1007/s00425-006-0290-4
pubmed: 16708225
Takemura K, Kamachi H, Kume A, Fujita T, Karahara I, Hanba YT (2017a) A hypergravity environment increases chloroplast size, photosynthesis, and plant growth in the moss Physcomitrella patens. J Plant Res 130:181–192
doi: 10.1007/s10265-016-0879-z
pubmed: 27896464
Takemura K, Watanabe R, Kameishi R, Sakaguchi N, Kamachi H, Kume A, Fujita T, Karahara I, Hanba YT (2017b) Hypergravity of 10 g changes plant growth, anatomy, chloroplast size, and photosynthesis in the moss Physcomitrella patens. Microgravity Sci Technol 29:467–473
doi: 10.1007/s12217-017-9565-6
Tamaoki D, Karahara I, Schreiber L, Wakasugi T, Yamada K, Kamisaka S (2006) Effects of hypergravity conditions on elongation growth and lignin formation in the inflorescence stem of Arabidopsis thaliana. J Plant Res 119:79–84
doi: 10.1007/s10265-005-0243-1
pubmed: 16328083
Tamaoki D, Karahara I, Nishiuchi T, De Oliveira S, Schreiber L, Wakasugi T, Yamada K, Yamaguchi K, Kamisaka S (2009) Transcriptome profiling in Arabidopsis inflorescence stems grown under hypergravity in terms of cell walls and plant hormones. Adv Space Res 44:245–253
doi: 10.1016/j.asr.2009.03.016
Tamaoki D, Karahara I, Nishiuchi T, Wakasugi T, Yamada K, Kamisaka S (2011) Involvement of auxin dynamics in hypergravity-induced promotion of lignin-related gene expression in Arabidopsis inflorescence stems. J Exp Bot 62:5463–5469
doi: 10.1093/jxb/err224
pubmed: 21841171
pmcid: 3223044
van Loon JJWA (2012) A large human centrifuge for exploration and exploitation research. Ann Kinesiologiae 3:107–121
Wade CE (2005) Responses across the gravity continuum: hypergravity to microgravity. Adv Space Biol Med 10:225–245
doi: 10.1016/S1569-2574(05)10009-4
pubmed: 16101110
Wakabayashi K, Nakano S, Soga K, Hoson T (2009) Cell wall-bound peroxidase activity and lignin formation in azuki bean epicotyls grown under hypergravity conditions. J Plant Physiol 166:947–954
doi: 10.1016/j.jplph.2008.12.006
pubmed: 19195738
Wakabayashi K, Soga K, Hoson T, Kotake T, Yamazaki T, Higashibata A, Ishioka N, Shimazu T, Fukui K, Osada I (2015) Suppression of hydroxycinnamate network formation in cell walls of rice shoots grown under microgravity conditions in space. PLoS ONE 10:e0137992
doi: 10.1371/journal.pone.0137992
pubmed: 26378793
pmcid: 4574559