Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Hypergravity – an evolutionarily novel environment, enhances the resilience of wheat to simulated drought and salinity stress

Mahamed Ashiq I A , Ravikumar Hosamani https://orcid.org/0000-0003-2636-3750 A * , Uday G. Reddy B , Ramesh S. Bhat A , Akbar S. MD C and Basavalingayya K Swamy https://orcid.org/0000-0001-7955-4994 D
+ Author Affiliations
- Author Affiliations

A Institute of Agricultural Biotechnology (IABT), University of Agricultural Sciences, Dharwad, Karnataka 580 005, India.

B AICRP on Wheat, MARS, University of Agricultural Sciences, Dharwad, Karnataka 580 005, India.

C ARS Dharwad (Hebballi Farm), University of Agricultural Sciences, Dharwad, Karnataka 580 005, India.

D ICAR-Indian Institute of Millet Research (IIMR), Hyderabad, Telangana 500 030, India.

* Correspondence to: hosamanirr@uasd.in

Handling Editor: Honghong Wu

Functional Plant Biology 51, FP24200 https://doi.org/10.1071/FP24200
Submitted: 14 August 2024  Accepted: 4 November 2024  Published: 29 November 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Previous research from our lab demonstrated that hypergravity that can be simulated using tabletop centrifuges, offering significant benefits to crop plants. Hypergravity enhances seedling vigor and growth parameters in bread wheat (Triticum aestivum) variety UAS 375. This enhanced root growth phenotype is believed to boost abiotic stress tolerance by facilitating deeper access to water and nutrients from the soil. This study investigated whether hypergravity-induced root growth enhancements could offer resilience to induced drought and salt stress, and whether such benefits would extend across other wheat genotypes. Hypergravity (10g for 12 h) conferred significant tolerance to simulated drought and salt stress, evidenced by improved seedling growth parameters as well as increased chlorophyll content and proline accumulation in response to hypergravity followed by stress challenge, compared to stress challenge alone. Liquid chromatography with tandem mass spectrometry indicated dynamic phytohormone modulation, and quantitative reverse transcription polymerase chain reaction data revealed significant alterations in the expression of genes associated with antioxidant enzymes and abiotic stresses. Thus, this study further supports the view that hypergravity boosts abiotic stress resilience through genetic and hormonal dynamics. Notably, these effects were consistent across genotypes. In conclusion, this study provides evidence that hypergravity can effectively improve resilience against seedling abiotic stresses in wheat.

Keywords: drought stress, gene expression, hypergravity, phytohormones, root and shoot growth regulation, salinity stress, seedling vigor, stress resilience, wheat.

References

Abdul-Baki AA, Anderson JD (1973) Vigor determination in soybean seed by multiple criteria. Crop Science 13(6), 630-633.
| Crossref | Google Scholar |

Ahmed HGM-D, Zeng Y, Shah AN, Yar MM, Ullah A, Ali M (2022a) Conferring of drought tolerance in wheat (Triticum aestivum L.) genotypes using seedling indices. Frontiers in Plant Science 13, 961049.
| Crossref | Google Scholar |

Ahmed K, Shabbir G, Ahmed M, Noor S, Mohi Ud Din A, Qamar M, Rehman N (2022b) Expression profiling of TaARGOS homoeologous drought responsive genes in bread wheat. Scientific Reports 12(1), 3595.
| Crossref | Google Scholar | PubMed |

Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285(5431), 1256-1258.
| Crossref | Google Scholar | PubMed |

Ashiq IM, Barthakur S, Gowtham TP (2024) Exploring the potential of heat priming in improving heat stress tolerance at anthesis stage in wheat (Triticum aestivum. L). Journal of Farm Sciences 37(01), 7-11.
| Crossref | Google Scholar |

Barnes JD, Balaguer L, Manrique E, Elvira S, Davison AW (1992) A reappraisal of the use of DMSO for the extraction and determination of chlorophylls a and b in lichens and higher plants. Environmental and Experimental Botany 32, 85-100.
| Crossref | Google Scholar |

Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205-207.
| Crossref | Google Scholar |

Bharti N, Pandey SS, Barnawal D, Patel VK, Kalra A (2016) Plant growth promoting rhizobacteria Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Scientific Reports 6, 34768.
| Crossref | Google Scholar | PubMed |

Brown AH, Dahl AO, Chapman DK (1976) Morphology of Arabidopsis grown under chronic centrifugation and on the clinostat. Plant Physiology 57(3), 358-364.
| Crossref | Google Scholar | PubMed |

Bruns HA, Croy LI (1985) Root volume and root dry weight measuring system for wheat cultivars. Cereal Research Communications 13(2/3), 177-183 Available at http://www.jstor.org/stable/23782998.
| Google Scholar |

Camaille M, Fabre N, Clément C, Ait Barka E (2021) Advances in wheat physiology in response to drought and the role of plant growth promoting rhizobacteria to trigger drought tolerance. Microorganisms 9(4), 687.
| Crossref | Google Scholar | PubMed |

Chen R, Rosen E, Masson PH (1999) Gravitropism in higher plants. Plant Physiology 120(2), 343-350.
| Crossref | Google Scholar | PubMed |

Chen L, Ren J, Shi H, Chen X, Zhang M, Pan Y, Fan J, Nevo E, Sun D, Fu J, Peng J (2013) Physiological and molecular responses to salt stress in wild emmer and cultivated wheat. Plant Molecular Biology Reporter 31, 1212-1219.
| Crossref | Google Scholar |

Dai K, Wang Y, Yan R, Shi Q, Wang Z, Yuan Y, Cheng H, Li S, Fan Y, Zhuang F (2009) Effects of microgravity and hypergravity on platelet functions. Thrombosis and Haemostasis 101(5), 902-910.
| Crossref | Google Scholar | PubMed |

Delavari PM, Baghizadeh A, Enteshari SH, Kalantari KM, Yazdanpanah A, Mousavi EA (2010) The effects of salicylic acid on some of biochemical and morphological characteristic of Ocimum basilicucm under salinity stress. Australian Journal of Basic and Applied Sciences 4(10), 4832-4845.
| Google Scholar |

Dudziak K, Zapalska M, Börner A, Szczerba H, Kowalczyk K, Nowak M (2019) Analysis of wheat gene expression related to the oxidative stress response and signal transduction under short-term osmotic stress. Scientific Reports 9(1), 2743.
| Crossref | Google Scholar | PubMed |

Frick EM, Strader LC (2018) Roles for IBA-derived auxin in plant development. Journal of Experimental Botany 69(2), 169-177.
| Crossref | Google Scholar | PubMed |

Fuertes-Aguilar J, Matilla AJ (2024) Transcriptional control of seed life: new insights into the role of the NAC family. International Journal of Molecular Sciences 25(10), 5369.
| Crossref | Google Scholar | PubMed |

Fukuda A, Nakamura A, Hara N, Toki S, Tanaka Y (2011) Molecular and functional analyses of rice NHX-type Na+/H+ antiporter genes. Planta 233(1), 175-188.
| Crossref | Google Scholar | PubMed |

Hosamani R, Swamy BK, Dsouza A, Sathasivam M (2023) Plant responses to hypergravity: a comprehensive review. Planta 257(1), 17.
| Crossref | Google Scholar | PubMed |

Hosamani R, Swamy BK, Sathasivam M, Dsouza A, Ashiq M (2024) Cocopeat supplementation negates lunar soil simulant-induced baneful phenotypic and biochemical changes in crop seedlings. Acta Astronautica 220, 416-426.
| Crossref | Google Scholar |

Hou P, Wang F, Luo B, Li A, Wang C, Shabala L, Ahmed HAI, Deng S, Zhang H, Song P, Zhang Y, Shabala S, Chen L (2021) Antioxidant enzymatic activity and osmotic adjustment as components of the drought tolerance mechanism in Carex duriuscula. Plants 10(3), 436.
| Crossref | Google Scholar | PubMed |

ISTA (1999) International rules for seed testing. Seed Science and Technology 27, 25-30.
| Google Scholar |

Jamshidi Goharrizi K, Baghizadeh A, Karami S, Nazari M, Afroushteh M (2023) Expression of the W36, P5CS, P5CR, MAPK3, and MAPK6 genes and proline content in bread wheat genotypes under drought stress. Cereal Research Communications 51(3), 545-556.
| Crossref | Google Scholar |

Mahpara S, Zainab A, Ullah R, Kausar S, Bilal M, Latif MI, Arif M, Akhtar I, Al-Hashimi A, Elshikh MS, Zivcak M, Zuan ATK (2022) The impact of PEG-induced drought stress on seed germination and seedling growth of different bread wheat (Triticum aestivum L.) genotypes. PLoS ONE 17(2), e0262937.
| Crossref | Google Scholar | PubMed |

Mega R, Meguro-Maoka A, Endo A, Shimosaka E, Murayama S, Nambara E, Seo M, Kanno Y, Abrams SR, Sato Y (2015) Sustained low abscisic acid levels increase seedling vigor under cold stress in rice (Oryza sativa L.). Scientific Reports 5, 13819.
| Crossref | Google Scholar | PubMed |

Mshelmbula B, Akomolafe G (2019) Preliminary investigation on the effect of centrifugal force on germination and early growth of maize (Zea mays L.). Transactions on Science and Technology 6(4), 328-333.
| Google Scholar |

Nasirzadeh L, Sorkhilaleloo B, Majidi Hervan E, Fatehi F (2021) Changes in antioxidant enzyme activities and gene expression profiles under drought stress in tolerant, intermediate, and susceptible wheat genotypes. Cereal Research Communications 49, 83-89.
| Crossref | Google Scholar |

Nazeer H, Rauf M, Gul H, Yaseen T, Shan AA, Rehman KU (2020) Salt stress affects germination and seedling establishment in different wheat (Triticum aestivum L.) varieties. Journal of Pure and Applied Agriculture 5(4), 42-51.
| Google Scholar |

Pan X, Welti R, Wang X (2008) Simultaneous quantification of major phytohormones and related compounds in crude plant extracts by liquid chromatography–electrospray tandem mass spectrometry. Phytochemistry 69(8), 1773-1781.
| Crossref | Google Scholar | PubMed |

Paul S, Roychoudhury A (2017) Effect of seed priming with spermine/spermidine on transcriptional regulation of stress-responsive genes in salt-stressed seedlings of an aromatic rice cultivar. Plant Gene 11, 133-142.
| Crossref | Google Scholar |

Pigolev A, Miroshnichenko D, Dolgov S, Savchenko T (2021) Regulation of sixth seminal root formation by jasmonate in Triticum aestivum L. Plants 10(2), 219.
| Crossref | Google Scholar | PubMed |

Pilet P-E, Saugy M (1987) Effect on root growth of endogenous and applied IAA and ABA: a critical reexamination. Plant Physiology 83(1), 33-38.
| Crossref | Google Scholar | PubMed |

Puyang X, An M, Xu L, Han L, Zhang X (2016) Protective effect of exogenous spermidine on ion and polyamine metabolism in Kentucky bluegrass under salinity stress. Horticulture, Environment, and Biotechnology 57, 11-19.
| Crossref | Google Scholar |

Rafique K, Gul A, Ahmad N, Mushtaq N (2024) Genome engineering in maize using CRISPR/CAS9 system. In ‘Targeted genome engineering via CRISPR/Cas9 in plants’. (Ed. A Gul) pp. 233–256. (Academic Press) 10.1016/B978-0-443-26614-0.00002-3

Rai MI (2016) Regulators of ethylene signaling in Arabidopsis thaliana: CTR1 and ARGOS family. Doctoral dissertation, Quaid-i-Azam University, Islamabad, Pakistan.

Sathasivam M, Hosamani R, Swamy BK, Kumaran G S (2021) Plant responses to real and simulated microgravity. Life Sciences in Space Research 28, 74-86.
| Crossref | Google Scholar | PubMed |

Sathasivam M, Swamy BK, Krishnan K, Sharma R, Nayak SN, Uppar DS, Hosamani R (2022) Insights into the molecular basis of hypergravity-induced root growth phenotype in bread wheat (Triticum aestivum L.). Genomics 114(2), 110307.
| Crossref | Google Scholar | PubMed |

Scherer GFE (2006) Halotolerance is enhanced in carrot callus by sensing hypergravity: influence of calcium modulators and cytochalasin D. Protoplasma 229(2-4), 149-154.
| Crossref | Google Scholar | PubMed |

Sharma P, Mishra S, Pandey B, Singh G (2023) Genome-wide identification and expression analysis of the NHX gene family under salt stress in wheat (Triticum aestivum L). Frontiers in plant science 14, 1266699.
| Crossref | Google Scholar | PubMed |

Sheoran S, Thakur V, Narwal S, Turan R, Mamrutha HM, Singh V, Tiwari V, Sharma I (2015) Differential activity and expression profile of antioxidant enzymes and physiological changes in wheat (Triticum aestivum L.) under drought. Applied Biochemistry and Biotechnology 177(6), 1282-1298.
| Crossref | Google Scholar | PubMed |

Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. International Journal of Molecular Sciences 16(6), 13561-13578.
| Crossref | Google Scholar | PubMed |

Sundararaj N, Nagaraju S, Ramu MV (1972) ‘Design and analysis of field experiments.’ Miscellaneous Series 22, p. 424440. (University of Agricultural Sciences: Bangalore)

Swamy BK, Hosamani R, Sathasivam M, Chandrashekhar SS, Reddy UG, Moger N (2021) Novel hypergravity treatment enhances root phenotype and positively influences physio-biochemical parameters in bread wheat (Triticum aestivum L.). Scientific Reports 11(1), 15303.
| Crossref | Google Scholar | PubMed |

Taj G, Agarwal P, Grant M, Kumar A (2010) MAPK machinery in plants: recognition and response to different stresses through multiple signal transduction pathways. Plant Signaling & Behaviour 5(11), 1370-1378.
| Crossref | Google Scholar |

Takemura K, Kamachi H, Kume A, Fujita T, Karahara I, Hanba YT (2017) A hypergravity environment increases chloroplast size, photosynthesis, and plant growth in the moss Physcomitrella patens. Journal of Plant Research 130(1), 181-192.
| Crossref | Google Scholar | PubMed |

Tanimoto E (2012) Tall or short? Slender or thick? A plant strategy for regulating elongation growth of roots by low concentrations of gibberellin. Annals of Botany 110(2), 373-381.
| Crossref | Google Scholar | PubMed |

Tiwari S, Lata C, Chauhan PS, Prasad V, Prasad M (2017) A functional genomic perspective on drought signalling and its crosstalk with phytohormone-mediated signalling pathways in plants. Current Genomics 18(6), 469-482.
| Crossref | Google Scholar | PubMed |

Van Loon JJWA, Krause J, Cunha H, Goncalves J, Almeida H, Schiller P (2008) The large diameter centrifuge, LDC, for life and physical sciences and technology. Life in Space for Life on Earth 553, 92.1-92.2.
| Google Scholar |

Vidyasagar PB, Jagtap JP, Dixit JP, Kamble SM, Dhepe AP (2014) Effects of short-term hypergravity exposure on germination, growth and photosynthesis of Triticum aestivum L. Microgravity Science and Technology 26(6), 375-384.
| Crossref | Google Scholar |

Waldron KW, Brett CT (1990) Effects of extreme acceleration on the germination, growth and cell wall composition of pea epicotyls. Journal of Experimental Botany 41(1), 71-77.
| Crossref | Google Scholar |

Yadav S, Kushwaha HR, Kumar K, Verma PK (2012) Comparative structural modeling of a monothiol GRX from chickpea: insight in iron–sulfur cluster assembly. International Journal of Biological Macromolecules 51(3), 266-273.
| Crossref | Google Scholar | PubMed |

Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B (2019) A Jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177(4), 942-956.e14.
| Crossref | Google Scholar | PubMed |