Inoculation of halotolerant plant-growth-promoting bacteria improved the growth of chia (Salvia hispanica L.) in saline and nonsaline soils
María Florencia Yañez-Yazlle
A B , Michelangelo Locatelli A B , Martín Moises Acreche C D , Verónica Beatriz Rajal A E F and Verónica Patricia Irazusta A B *
A
B
C
D
E
F
Abstract
Chia (Salvia hispanica L.), a nutrient-rich crop with potential application in different industries, is sensitive to salinity. Halotolerant plant-growth promoting bacteria could be a biotechnological strategy to increase chia’s salinity tolerance.
The aim of this study was to determine the morphological and physiological response of chia plants inoculated with free-living halotolerant plant-growth promoting bacteria and grown in saline soils under greenhouse conditions.
A total of 15 bacterial treatments were inoculated to plants potted in soils with three electrical conductivity levels: 0.5, 4, and 6 dS m−1. Mortality and morphological and physiological parameters were evaluated. The measured variables were used to calculate a relative growth index.
Bacterial inoculation had a positive effect on plants at 4 dS m−1. Plants inoculated with Pseudomonas sp. AN23, Kushneria sp. T3.7, and C6 (Halomonas sp. 3R12 + Micrococcus luteus SA211) exhibited the best morphological and physiological performance (51% longer shoots, up to 90% heavier roots and up to 400% higher photosynthetic rate than control plants). Moreover, plants inoculated with Kushneria sp. T3.7 and C5 (Halomonas sp. 3R12 + Pseudomonas sp. AN23) showed significant increase in stomatal conductance and transpiration rate (up to 12 times) and in proline production (up to 345 μg g−1 leaf fresh weight) with respect to control plants (8 μg g−1 leaf fresh weight) under saline conditions.
The analysed extremophilic plant-growth promoting bacteria enhanced growth and stress tolerance in chia, a salt-sensitive crop.
Free-living plant-growth promoting bacteria isolated from hypersaline environments have potential for bioinoculant formulation for salinity-sensitive crops.
Keywords: beneficial bacteria, photosynthesis, physiological status, saline stress, shoot and root dry weight, shoot and root length, stomatal conductance, transpiration.
References
Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7, 18.
| Crossref | Google Scholar |
Afrangan F, Kazemeini SA, Alinia M, Mastinu A (2023) Glomus versiforme and Micrococcus yunnanensis reduce the negative effects of salinity stress by regulating the redox state and ion homeostasis in Brassica napus L. crops. Biologia 78, 3049-3061.
| Crossref | Google Scholar |
Ahamd M, Zahir ZA, Nadeem SM, Nazli F, Jamil M, Jamshaid MU (2014) Physiological response of mung bean to rhizobium and pseudomonas based biofertilizers under salinity stress. Pakistan Journal of Agricultural Research 51, 555-562.
| Google Scholar |
Amato M, Caruso MC, Guzzo F, Galgano F, Commisso M, Bochicchio R, Labella R, Favati F (2015) Nutritional quality of seeds and leaf metabolites of chia (Salvia hispanica L.) from Southern Italy. European Food Research and Technology 241, 615-625.
| Crossref | Google Scholar |
Armada E, Roldán A, Azcon R (2014) Differential activity of autochthonous bacteria in controlling drought stress in native Lavandula and Salvia plants species under drought conditions in natural arid soil. Microbial Ecology 67, 410-420.
| Crossref | Google Scholar | PubMed |
Badawy IH, Hmed AA, Sofy MR, Al-Mokadem AZ (2022) Alleviation of cadmium and nickel toxicity and phyto-stimulation of tomato plant L. by endophytic Micrococcus luteus and Enterobacter cloacae. Plants 11, 2018.
| Crossref | Google Scholar |
Basu A, Prasad P, Das SN, Kalam S, Sayyed RZ, Reddy MS, Enshasy HE (2021) Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability 13, 1140.
| 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 |
Bekkaye M, Baha N, Behairi S, MariaPerez-Clemente R, Kaci Y (2023) Impact of bio-inoculation with halotolerant rhizobacteria on growth, physiological, and hormonal responses of durum wheat under salt stress. Journal of Plant Growth Regulation 42, 6549-6564.
| Crossref | Google Scholar |
Bilalis DJ, Roussis I, Kakabouki I, Karydogianni S (2020) Effects of salinity and arbuscular mycorrhizal fungi (AMF) on root growth development and productivity of Chia (Salvia hispanica L.), a promising salt-tolerant crop, under mediterranean conditions. In ‘Handbook of halophytes: from molecules to ecosystems towards biosaline agriculture’. (Ed. MN Grigore) p. 1–30. (Springer)
Bochicchio R, Rossi R, Labella R, Bitella G, Perniola M, Amato M (2015) Effect of sowing density and nitrogen top-dress fertilisation on growth and yield of chia (Salvia hispanica L.) in a Mediterranean environment: first results. Italian Journal of Agronomy 10, 163-166.
| Crossref | Google Scholar |
Brandán JP, Curti RN, Acreche MM (2020) Developmental responses of chia (Salvia hispanica) to variations in thermo-photoperiod: impact on subcomponents of grain yield. Crop & Pasture Science 71, 183-189.
| Crossref | Google Scholar |
Busilacchi H, Qüesta M, Wagner A, Cabezas C, Bresó A (2018) Características del mercado minorista de chia y colza en la ciudad de Rosario. Factibilidad de producción agroecológica y agregado de valor. Agromensajes 20-24.
| Google Scholar |
Costa AAd, Paiva EPd, Torres SB, Neta MLdS, Pereira KTdO, Leite MdS, Sá FVdS (2021) Seed priming improves Salvia hispanica L. seed performance under salt stress. Acta Scientiarum. Agronomy 43, e52006.
| Crossref | Google Scholar |
Food and Agriculture Organizaton of the United Nations (FAO) (2010) Proceedings of the Global Forum on Salinization and Climate Change (GFSCC2010), Valencia, 25–29 October 2010. (Ed. RP Thomas) pp. 25–29. (Food and Agriculture Organization: Rome, Italy) Available at https://openknowledge.fao.org/server/api/core/bitstreams/524101c5-7b5b-4a0c-b0d8-1dfa81bc7461/content
Gamalero E, Glick BR (2022) Recent advances in bacterial amelioration of plant drought and salt stress. Biology 11, 437.
| Crossref | Google Scholar | PubMed |
Hassan TU, Bano A, Naz I (2018) Halophyte root powder: an alternative biofertilizer and carrier for saline land. Soil Science and Plant Nutrition 64, 653-661.
| Crossref | Google Scholar |
Heuer B, Yaniv Z, Ravina I (2002) Effect of late salinization of chia (Salvia hispanica), stock (Matthiola tricuspidata) and evening primrose (Oenothera biennis) on their oil content and quality. Industrial Crops and Products 15, 163-167.
| Crossref | Google Scholar |
Ilangumaran G, Smith DL (2017) Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Frontiers in Plant Science 8, 1768.
| Crossref | Google Scholar |
Ixtaina VY, Nolasco SM, Tomás MC (2008) Physical properties of chia (Salvia hispanica L.) seeds. Industrial Crops and Products 28, 286-293.
| Crossref | Google Scholar |
Izadi Y, Moosavi SA, Gharineh MH (2022) Salinity affects eco-physiological aspects and biochemical compositions in chia (Salvia hispanica L.) during germination and seedling growth. Scientia Horticulturae 306, 111461.
| Crossref | Google Scholar |
Knez Hrncic M, Ivanovski M, Cör D, Željko K (2020) Chia seeds (Salvia Hispanica L.): an overview – phytochemical profile, isolation methods, and application. Molecules 25, 11.
| Crossref | Google Scholar |
Lovelli S, Valerio M, Phillips TD, Amato M (2019) Water use efficiency, photosynthesis and plant growth of chia (Salvia hispanica L.): a glasshouse experiment. Acta Physiologiae Plantarum 41, 3.
| Crossref | Google Scholar |
Mansour MMF, Ali EF (2017) Evaluation of proline functions in saline conditions. Phytochemistry 140, 52-68.
| Crossref | Google Scholar | PubMed |
Moghith WMA, Youssef ASM, El-Wahab MAA, Mohamed YFY, Eman MAE-G (2020) Effect of saline water stress in the presence of silicon foliar application on growth, productivity and chemical constituents of chia (Salvia hispanica L.) under Egyptian condition. Asian Plant Research Journal 4, 28-45.
| Crossref | Google Scholar |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiologia Plantarum 15, 473-497.
| Crossref | Google Scholar |
Negrão S, Schmöckel SM, Tester M (2017) Evaluating physiological responses of plants to salinity stress. Annals of Botany 119, 1-11.
| Crossref | Google Scholar | PubMed |
Okon OG (2019) Effect of salinity on physiological processes in plants. In ‘Microorganisms in saline environments: strategies and functions.’ (Eds B Giri, A Varma) pp. 237–262. (Springer Nature: Switzerland AG) doi:10.1007/978-3-030-18975-4_10
Ouzounidou G, Skiada V, Papadopoulou KK, Stamatis N, Kavvadias V, Eleftheriadis E, Gaitis F (2015) Effects of soil pH and arbuscular mycorrhiza (AM) inoculation on growth and chemical composition of chia (Salvia hispanica L.) leaves. Brazilian Journal of Botany 38, 487-495.
| Crossref | Google Scholar |
Paiva EPd, Torres SB, Alves TRC, Sá FVdS, Leite MDS, Dombroski JLD (2018) Germination and biochemical components of Salvia hispanica L. seeds at different salinity levels and temperatures. Acta Scientiarum. Agronomy 40, 39396.
| Crossref | Google Scholar |
Rabhi NEH, Silini A, Cherif-Silini H, Yahiaoui B, Lekired A, Robineau M, Esmaeel Q, Jacquard C, Vaillant-Gaveau N, Clément C, Aït Barka E, Sanchez L (2018) Pseudomonas knackmussii MLR6, a rhizospheric strain isolated from halophyte, enhances salt tolerance in Arabidopsis thaliana. Journal of Applied Microbiology 125, 1836-1851.
| Crossref | Google Scholar |
Raimondi G, Rouphael Y, Di Stasio E, Napolitano F, Clemente G, Maiello R, Giordano M, De Pascale S (2017) Evaluation of Salvia hispanica performance under increasing salt stress conditions. Acta Horticulturae 1170, 703-708.
| Crossref | Google Scholar |
Saghafi D, Delangiz N, Lajayer BA, Ghorbanpour M (2019) An overview on improvement of crop productivity in saline soils by halotolerant and halophilic PGPRs. 3 Biotech 9, 261.
| Crossref | Google Scholar |
Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez J-Y, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676-682.
| Crossref | Google Scholar | PubMed |
Sharma A, Kumar V, Shahzad B, Ramakrishnan M, Singh Sidhu GP, Bali AS, Handa N, Kapoor D, Yadav P, Khanna K, Bakshi P, Rehman A, Kohli SK, Khan EA, Parihar RD, Yuan H, Thukral AK, Bhardwaj R, Zheng B (2020) Photosynthetic response of plants under different abiotic stresses: a review. Journal of Plant Growth Regulation 39, 509-531.
| Crossref | Google Scholar |
Shultana R, Kee Zuan AT, Yusop MR, Saud HM (2020) Characterization of salt-tolerant plant growth-promoting rhizobacteria and the effect on growth and yield of saline-affected rice. PLoS ONE 15, e0238537.
| Crossref | Google Scholar | PubMed |
Silva H, Valenzuela C, Garrido M, Acevedo E, Campos S, Silva P, Morales-Salinas L (2021) Pressure–volume curve traits of chia (Salvia hispanica L.): an assessment of water-stress tolerance under field conditions. Irrigation Science 39, 789-801.
| Crossref | Google Scholar |
Sosa A, Ruiz G, Rana J, Gordillo G, West H, Sharma M, Raul XL, Robles R (2017) Chia crop (Salvia hispanica L.): its history and importance as a source of polyunsaturated fatty acids Omega-3 around the World: a review. Journal of Crop Research and Fertilizers 1, 1-9.
| Crossref | Google Scholar |
Stefanello R, Viana BB, Goergen PCH, Neves LAS, Nunes UR (2020) Germination of chia seeds submitted to saline stress. Brazilian Journal of Biology 80, 285-289.
| Crossref | Google Scholar |
Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends in Plant Science 15, 89-97.
| Crossref | Google Scholar | PubMed |
Szymańska S, Dąbrowska GB, Tyburski J, Niedojadło K, Piernik A, Hrynkiewicz K (2019) Boosting the Brassica napus L. tolerance to salinity by the halotolerant strain Pseudomonas stutzeri ISE12. Environmental and Experimental Botany 163, 55-68.
| Crossref | Google Scholar |
Szymańska S, Tyburski J, Piernik A, Sikora M, Mazur J, Katarzyna H (2020) Raising beet tolerance to salinity through bioaugmentation with halotolerant endophytes. Agronomy 10, 1571.
| Crossref | Google Scholar |
Szymańska S, Lis MI, Piernik A, Hrynkiewicz K (2022) Pseudomonas stutzeri and Kushneria marisflavi alleviate salinity stress-associated damages in barley, lettuce, and sunflower. Frontiers in Microbiology 13, 788893.
| Crossref | Google Scholar |
Tamayo PR, Bonjoch NP (2001) Free proline quantification. In ‘Handbook of plant ecophysiology techniques’. (Ed. MJ Reigosa Roger) pp. 365–382. (Springer) doi:10.1007/0-306-48057-3_22
Timmusk S, Behers L, Muthoni J, Muraya A, Aronsson A-C (2017) Perspectives and challenges of microbial application for crop improvement. Frontiers in Plant Science 8, 49.
| Crossref | Google Scholar |
Toubali S, Meddich A (2023) Role of combined use of mycorrhizae fungi and plant growth promoting rhizobacteria in the tolerance of quinoa plants under salt stress. Gesunde Pflanzen 75, 1855-1869.
| Crossref | Google Scholar |
Villarroel JA (1988) Manual práctico para la interpretación de Análisis de Suelos En Laboratorio. Serie Técnica No. 10. Edición AGROCO, Cochabamba-Bolivia. Available at https://es.scribd.com/doc/253867585/Manual-Practico-Para-La-Interpretacion-de-Analisisde-Suelos-en-Laboratorio
Win KT, Tanaka F, Okazaki K, Ohwaki Y (2018) The ACC deaminase expressing endophyte Pseudomonas spp. enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance, and ionic balance in tomato plants. Plant Physiology and Biochemistry 127, 599-607.
| Crossref | Google Scholar | PubMed |
Yañez-Yazlle MF, Romano-Armada N, Acreche MM, Rajal VB, Irazusta VP (2021a) Halotolerant bacteria isolated from extreme environments induce seed germination and growth of chia (Salvia hispanica L.) and quinoa (Chenopodium quinoa Willd.) under saline stress. Ecotoxicology and Environmental Safety 218, 112273.
| Crossref | Google Scholar | PubMed |
Yañez-Yazlle MF, Romano-Armada N, Rajal VB, Irazusta VP (2021b) Amelioration of saline stress on chia (Salvia hispanica L.) seedlings inoculated with halotolerant plant growth-promoting bacteria isolated from hypersaline environments. Frontiers in Agronomy 3, 665798.
| Crossref | Google Scholar |
Younis ME, Rizwan M, Tourky SMN (2021) Assessment of early physiological and biochemical responses in chia (Salvia hispanica L.) sprouts under salt stress. Acta Physiologiae Plantarum 43, 121.
| Crossref | Google Scholar |
Zhou N, Zhao S, Tian C-Y (2017) Effect of halotolerant rhizobacteria isolated from halophytes on the growth of sugar beet (Beta vulgaris L.) under salt stress. FEMS Microbiology Letters 364, fnx091.
| Crossref | Google Scholar |
