Impact of irrigation water deficit on two tomato genotypes grown under open field conditions: From the root-associated microbiota to the stress responses

Submitted: 29 June 2022
Accepted: 30 August 2022
Published: 13 September 2022
Abstract Views: 1074
PDF: 688
APPENDIX 1: 254
APPENDIX 2: 296
HTML: 234
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

Authors

In the context of the climate change scenario in the Mediterranean, natural root-microorganism associations have an impact on the resilience and productivity of crops, and the exploitation of these interactions represents innovative, cost-effective and sustainable crop adaptation strategies. An open field experiment with two commercial Italian tomato cultivars was performed. The soil bacterial communities associated with the two commercial Italian tomato genotypes were characterized alongside their physiological and molecular responses under wellwatered and moderate water deficit (100% and 75% of crop evapotranspiration) treatments. The two genotypes showed contrasting responses to water deficit, primarily through diverse rhizosphere microbiota recruitment under the two irrigation treatments.

Highlights
- Two tomato genotypes were studied under water deficit in a pilot field trial.
- The two genotypes responded differently to water stress from eco-physiological and transcriptomic points of view.
- The two genotypes recruited diverse root-associated microbiota, particularly under water deficit.

Dimensions

Altmetric

PlumX Metrics

Downloads

Download data is not yet available.

Citations

Allen RG, Pereira LS, Raes D, Smith M, 1998. Crop evapotranspiration. Guidelines for Computing Crop Water Requirements FAO Irrigation and Drainage; Paper No. 56; FAO: Rome, Italy, 1998.
Arji I, Hassany B, Ghamarnia H, 2016. The effects of water stress on apple qualities and quantities (Golden delicious variety). J. Hortic. Sci. 29:610-20.
Ashraf M, Hasnain S, Berge O, Mahmood T, 2004. Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol. Fert. Soils 40:157-62. DOI: https://doi.org/10.1007/s00374-004-0766-y
Berendsen RL, Pieterse CM, Bakker PA, 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17:478-86.
Breitkreuz C, Herzig L, Buscot F, Reitz T, Tarkka M, 2021. Interactions between soil properties, agricultural management and cultivar type drive structural and functional adaptations of the wheat rhizosphere microbiome to drought. Env. Microbiol. 23:5866-82. DOI: https://doi.org/10.1111/1462-2920.15607
Brilli F, Pollastri S, Raio A, Baraldi R, Neri L, Bartolini P, Balestrini R, 2019. Root colonization by Pseudomonas chlororaphis primes tomato (Lycopersicum esculentum) plants for enhanced tolerance to water stress. J. Plant Physiol. 232:82-93. DOI: https://doi.org/10.1016/j.jplph.2018.10.029
Brunetti C, Savi T, Nardini A, Loreto F, Gori A, Centritto M, 2020. Changes in abscisic acid content during and after drought are related to carbohydrate mobilization and hydraulic recovery in poplar stems. Tree Physiol. 40:1043-57. DOI: https://doi.org/10.1093/treephys/tpaa032
Brunetti C, Saleem AR, Della Rocca G, Emiliani G, De Carlo A, Balestrini R, Centritto M, 2021. Effects of plant growth-promoting rhizobacteria strains producing ACC deaminase on photosynthesis, isoprene emission, ethylene formation and growth of Mucuna pruriens (L.) DC. in response to water deficit. J. Biotech. 331:53-62. DOI: https://doi.org/10.1016/j.jbiotec.2021.03.008
Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, Schulze-Lefert P, 2015. Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392-403. DOI: https://doi.org/10.1016/j.chom.2015.01.011
Calleja-Cabrera J, Boter M, Oñate-Sánchez L, Pernas M, 2020. Root growth adaptation to climate change in crops. Front. Plant Sci. 11:544. DOI: https://doi.org/10.3389/fpls.2020.00544
Cartelat A, Cerovic ZG, Goulas Y, Meyer S, Lelarge C, Prioul JL, Moya I, 2005. Optically assessed contents of leaf polyphenolics and chlorophyll as indicators of nitrogen deficiency in wheat (Triticum aestivum L.). Field Crops Res. 91:35-49. DOI: https://doi.org/10.1016/j.fcr.2004.05.002
Centritto M, Loreto F, Chartzoulakis K, 2003. The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt-stressed olive saplings. Plant Cell Environ. 26:585-94. DOI: https://doi.org/10.1046/j.1365-3040.2003.00993.x
Cheng Z, Lei S, Li Y, Huang W, Ma R, Xiong J, Tian B, 2020. Revealing the variation and stability of bacterial communities in tomato rhizosphere microbiota. Microorganisms 8:170.
Chialva M, Salvioli di Fossalunga A, Daghino S, Ghignone S, Bagnaresi P, Chiapello M, ... Bonfante P, 2018. Native soils with their microbiotas elicit a state of alert in tomato plants. New Phytol. 220:1296-308.
Chialva M, Ghignone S, Novero M, Hozzein WN, Lanfranco L, Bonfante P, 2019. Tomato RNA-seq data mining reveals the taxonomic and functional diversity of root associated microbiota. Microorganisms 8:38. DOI: https://doi.org/10.3390/microorganisms8010038
Chitarra W, Pagliarani C, Maserti B, Lumini E, Siciliano I, Cascone P, Guerrieri E, 2016. Insights on the impact of arbuscular mycorrhizal symbiosis on tomato tolerance to water stress. Plant Physiol. 171:1009-23.
Chong J, Liu P, Zhou G, Xia J, 2020. Using MicrobiomeAnalyst for comprehensive statistical, functional, and meta-analysis of microbiome data. Nat. Protoc. 15:799-821.
Christou A, Kyriacou MC, Georgiadou EC, Papamarkou R, Hapeshi E, Karaolia P, Michael C, Fotopoulos V, Fatta-Kassinos D, 2019. Uptake and bioaccumulation of three widely prescribed pharmaceutically active compounds in tomato fruits and mediated effects on fruit quality attributes. Sci. Total Environ. 647:1169-78.
Coleman HD, Yan J, Mansfield SD, 2009. Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc. Natl. Acad. Sci. U. S. A. 106:13118-23. DOI: https://doi.org/10.1073/pnas.0900188106
Conti V, Cantini C, Romi M, Cesare MM, Parrotta L, Del Duca S, Cai G, 2022. Distinct tomato cultivars are characterized by a differential pattern of biochemical responses to drought stress. Int. J. Mol. Sci. 23:5412.
Cordovez V, Schop S, Hordijk K, Dupré de Boulois H, Coppens F, Hanssen I, Carrión VJ, 2018. Priming of plant growth promotion by volatiles of root-associated Microbacterium spp. App. Env. Microbiol. 84:e01865-18.
Cordovez V, Rotoni C, Dini-Andreote F, Oyserman B, Carrión VJ, Raaijmakers JM, 2021.Successive plant growth amplifies genotype-specific assembly of the tomato rhizosphere microbiome. Sci. Total Environ. 772:144825. DOI: https://doi.org/10.1016/j.scitotenv.2020.144825
Corrado G, Sasso R, Pasquariello M, Iodice L, Carretta A, Cascone P, Rao R, 2007. Systemin regulates both systemic and volatile signaling in tomato plants. J. Chem. Ecol. 33:669-81. DOI: https://doi.org/10.1007/s10886-007-9254-9
Costa JM, Heuvelink E, 2018. The global tomato industry. In: E. Heuvelink (Ed.), Tomatoes. CAB International, Wallingford, pp 1-26. DOI: https://doi.org/10.1079/9781780641935.0001
Costa JM, Marques da Silva J, Pinheiro C, Barón M, Mylona P, Centritto M, Oliveira MM, 2019. Opportunities and limitations of crop phenotyping in southern European countries. Front. Plant Sci. 10:1125. DOI: https://doi.org/10.3389/fpls.2019.01125
Cramer W, Guiot J, Fader M, Garrabou J, Gattuso JP, Iglesias A, Xoplaki E, 2018. Climate change and interconnected risks to sustainable development in the Mediterranean. Nature Clim. Change 8:972-80. DOI: https://doi.org/10.1038/s41558-018-0299-2
Davies WJ, Bacon MA, Stuart Thompson D, Sobeih W, González Rodríguez L, 2000. Regulation of leaf and fruit growth in plants growing in drying soil: exploitation of the plants’ chemical signalling system and hydraulic architecture to increase the efficiency of water use in agriculture. J. Exp. Bot. 51:1617-26. DOI: https://doi.org/10.1093/jexbot/51.350.1617
de Vries FT, Griffiths RI, Knight CG, Nicolitch O, Williams A, 2020. Harnessing rhizosphere microbiomes for drought-resilient crop production. Science 368:270-74. DOI: https://doi.org/10.1126/science.aaz5192
Digilio MC, Corrado G, Sasso R, Coppola V, Iodice L, Pasquariello M, Guerrieri E, 2010. Molecular and chemical mechanisms involved in aphid resistance in cultivated tomato. New Phytol. 18:1089-101.
Dodds PN, Rathjen JP, 2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nat. Rev. Genet. 11:539-48.
Du Y, Zhao Q, Chen L, Yao X, Zhang W, Zhang B, Xie F, 2020. Effect of drought stress on sugar metabolism in leaves and roots of soybean seedlings. Plant Physiol. Biochem. 146:1-12. DOI: https://doi.org/10.1016/j.plaphy.2019.11.003
Durand M, Brendel O, Buré C, Le Thiec D, 2019. Altered stomatal dynamics induced by changes in irradiance and vapour-pressure deficit under drought: impacts on the whole‐plant transpiration efficiency of poplar genotypes. New Phytol. 222:1789-802. DOI: https://doi.org/10.1111/nph.15710
Edwards J, Johnson C, Santos-Medellín C, Lurie E, Podishetty NK, Bhatnagar S, Sundaresan V, 2015. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl. Acad. Sci. U. S. A. 112:E911-20. DOI: https://doi.org/10.1073/pnas.1414592112
Egea I, Albaladejo I, Meco V, Morales B, Sevilla A, Bolarin MC, Flores FB, 2018. The drought-tolerant Solanum pennellii regulates leaf water loss and induces genes involved in amino acid and ethylene/jasmonate metabolism under dehydration. Sci. Rep. 8:1-14. DOI: https://doi.org/10.1038/s41598-018-21187-2
Escudero-Martinez C, Bulgarelli D, 2019. Tracing the evolutionary routes of plant-microbiota interactions. Curr. Op. Microbiol. 49:34-40. DOI: https://doi.org/10.1016/j.mib.2019.09.013
Expósito-Rodríguez M, Borges AA, Borges-Pérez A, Pérez JA, 2008. Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol. 8:1-12. DOI: https://doi.org/10.1186/1471-2229-8-131
Fitzpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MT, 2018. Assembly and ecological function of the root microbiome across angiosperm plant species. Proc. Natl. Acad. Sci. U. S. A. 115:E1157-65.
Flexas J, Niinemets Ü, Gallé A, Barbour MM, Medrano H, 2013. Diffusional conductances to CO2 as a target for increasing photosynthesis and photosynthetic water-use efficiency. Photosynthesis Res. 117:45-59. DOI: https://doi.org/10.1007/s11120-013-9844-z
Franco-Correa M, Chavarro-Anzola V, 2016. Actinobacteria as plant growth promoting rhizobacteria. In: D. Dhanasekaran, Y. Jiang (Eds.), Actinobacteria - Basics and Biotechnological Application. IntechOpen, London, pp 249-70. DOI: https://doi.org/10.5772/61291
Franks PJ, Farquhar GD, 2007. The mechanical diversity of stomata and its significance in gas-exchange control. Plant Physiol. 143:78-87. DOI: https://doi.org/10.1104/pp.106.089367
Genty B, Briantais JM, Baker NR, 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochem. Biophys. Acta - General Subject 990:87-92. DOI: https://doi.org/10.1016/S0304-4165(89)80016-9
Gerardin T, Douthe C, Flexas J, Brendel O, 2018. Shade and drought growth conditions strongly impact dynamic responses of stomata to variations in irradiance in Nicotiana tabacum. Environ. Exp. Bot. 153:188-97. DOI: https://doi.org/10.1016/j.envexpbot.2018.05.019
Giannakoula AE, Ilias IF, 2013. The effect of water stress and salinity on growth and physiology of tomato (Lycopersicon esculentum Mil.). Arch. Biol. Sci. 65:611-20. DOI: https://doi.org/10.2298/ABS1302611G
Głowacka K, Kromdijk J, Kucera K, Xie J, Cavanagh AP, Leonelli L, Long SP, 2018. Photosystem II Subunit S overexpression increases the efficiency of water use in a field-grown crop. Nature Comm. 9:1-9. DOI: https://doi.org/10.1038/s41467-018-03231-x
Haworth M, Marino G, Centritto M, 2018a. An introductory guide to gas exchange analysis of photosynthesis and its application to plant phenotyping and precision irrigation to enhance water use efficiency. J. Water Clim. Change 9:786-808.
Haworth M, Marino G, Cosentino SL, Brunetti C, De Carlo A, Avola G, Centritto M, 2018b. Increased free abscisic acid during drought enhances stomatal sensitivity and modifies stomatal behaviour in fast growing giant reed (Arundo donax L.). Env. Exp. Bot. 147:116-24. DOI: https://doi.org/10.1016/j.envexpbot.2017.11.002
Iovieno P, Punzo P, Guida G, Mistretta C, Van Oosten MJ, Nurcato R, Grillo S, 2016. Transcriptomic changes drive physiological responses to progressive drought stress and rehydration in tomato. Front. Plant Sci. 7:371. DOI: https://doi.org/10.3389/fpls.2016.00371
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Ladle RJ, 2016. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 38:1-11. DOI: https://doi.org/10.1007/s11738-016-2113-y
Killi D, Haworth M, 2017. Diffusive and metabolic constraints to photosynthesis in quinoa during drought and salt stress. Plants 6:49. DOI: https://doi.org/10.3390/plants6040049
Kissoudis C, Chowdhury R, van Heusden S, van de Wiel C, Finkers R, Visser RG, van der Linden G, 2015. Combined biotic and abiotic stress resistance in tomato. Euphytica 202:317-32.
Kolton M, Erlacher A, Berg G, Cytryn E, 2016. The flavobacterium genus in the plant holobiont: ecological, physiological, and applicative insights. In: S. Castro-Sowinski (Ed.), Microbial models: from environmental to industrial sustainability. Microorganisms for Sustainability, vol 1. Springer, Singapore, pp 189-207. DOI: https://doi.org/10.1007/978-981-10-2555-6_9
Kumar M, Kour D, Yadav AN, Saxena R, Rai PK, Jyoti A, Tomar RS, 2019. Biodiversity of methylotrophic microbial communities and their potential role in mitigation of abiotic stresses in plants. Biologia 74:287-308. DOI: https://doi.org/10.2478/s11756-019-00190-6
Landi S, De Lillo A, Nurcato R, Grillo S, Esposito S, 2017. In-field study on traditional Italian tomato landraces: the constitutive activation of the ROS scavenging machinery reduces effects of drought stress. Plant Physiol. Biochem. 118:150-60. DOI: https://doi.org/10.1016/j.plaphy.2017.06.011
Larousse M, Rancurel C, Syska C, Palero F, Etienne C, Nesme X, Galiana E, 2017. Tomato root microbiota and Phytophthora parasitica-associated disease. Microbiome 5:1-11. DOI: https://doi.org/10.1186/s40168-017-0273-7
Lee SM, Kong HG, Song GC, Ryu CM, 2021. Disruption of Firmicutes and Actinobacteria abundance in tomato rhizosphere causes the incidence of bacterial wilt disease. ISME J. 15:330-47.
Lee S, Kim Y, Kim JM, Chu B, Joa JH, Sang MK, Weon HY, 2019. A preliminary examination of bacterial, archaeal, and fungal communities inhabiting different rhizocompartments of tomato plants under real-world environments. Sci. Rep. 9:1-15. DOI: https://doi.org/10.1038/s41598-019-45660-8
Lei S, Xu X, Cheng Z, Xiong J, Ma R, Zhang L, Tian B, 2019. Analysis of the community composition and bacterial diversity of the rhizosphere microbiome across different plant taxa. MicrobiologyOpen 8:e00762. DOI: https://doi.org/10.1002/mbo3.762
Lobos TE, Retamales JB, Ortega-Farías S, Hanson EJ, López-Olivari R, Mora ML, 2016. Pre-harvest regulated deficit irrigation management effects on post-harvest quality and condition of V. corymbosum fruits cv. Brigitta. Sci. Hort. 207:152-9. DOI: https://doi.org/10.1016/j.scienta.2016.05.022
López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ, Bouwmeester H, 2010. Does abscisic acid affect strigolactone biosynthesis? New Phytol. 187:343-54. DOI: https://doi.org/10.1111/j.1469-8137.2010.03291.x
Loriaux S, Avenson T, Welles J, McDermitt D, Eckles R, Riensche B, Genty B, 2013. Closing in on maximum yield of chlorophyll fluorescence using a single multiphase flash of sub-saturating intensity. Plant Cell Environ. 36:1755-70. DOI: https://doi.org/10.1111/pce.12115
Machado J, Fernandes APG, Fernandes TR, Heuvelink E, Vasconcelos MW, Carvalho SMP, 2022. Drought and nitrogen stress effects and tolerance mechanisms in tomato: a review. In: V. Kumar, A. Kumar Srivastava, P. Suprasanna (Eds.), Plant nutrition and food security in the era of climate change. Academic Press, pp 315-59.
Marino G, Haworth M, Scartazza A, Tognetti R, Centritto M, 2020. A comparison of the variable j and carbon-isotopic composition of sugars methods to assess mesophyll conductance from the leaf to the canopy scale in drought-stressed cherry. Int. J. Mol. Sci. 21:1222.
Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R, 2010. Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232:533-43. DOI: https://doi.org/10.1007/s00425-010-1196-8
McLoughlin F, Galvan‐Ampudia CS, Julkowska MM, Caarls L, Van Der Does D, Laurière C, Testerink C, 2012. The Snf1‐related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant J. 72:436-49. DOI: https://doi.org/10.1111/j.1365-313X.2012.05089.x
McMurdie PJ, Holmes S, 2013. phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8:e61217. DOI: https://doi.org/10.1371/journal.pone.0061217
Miller SA, Smith GS, Boldingh HL, Johansson A, 1998. Effects of water stress on fruit quality attributes of kiwifruit. Ann. Bot. 81:73-81. DOI: https://doi.org/10.1006/anbo.1997.0537
Naylor D, DeGraaf S, Purdom E, Coleman-Derr D, 2017. Drought and host selection influence bacterial community dynamics in the grass root microbiome. ISME J. 11:2691-704. DOI: https://doi.org/10.1038/ismej.2017.118
Naylor D, Coleman-Derr D, 2018. Drought stress and root-associated bacterial communities. Front. Plant Sci. 8:2223.
Nemeskéri E, Neményi A, Bőcs A, Pék Z, Helyes L, 2019. Physiological factors and their relationship with the productivity of processing tomato under different water supplies. Water 11:586. DOI: https://doi.org/10.3390/w11030586
Ngalimat MS, Mohd Hata E, Zulperi D, Ismail SI, Ismail MR, Mohd Zainudin N AI, Yusof MT, 2021. Plant growth-promoting bacteria as an emerging tool to manage bacterial rice pathogens. Microorganisms 9:682. DOI: https://doi.org/10.3390/microorganisms9040682
Nuruddin MM, Madramootoo CA, Dodds GT, 2003. Effects of water stress at different growth stages on greenhouse tomato yield and quality. HortSci. 38:1389-93. DOI: https://doi.org/10.21273/HORTSCI.38.7.1389
Pérez‐Pastor A, Ruiz‐Sánchez MC, Martínez JA, Nortes PA, Artés F, Domingo R, 2007. Effect of deficit irrigation on apricot fruit quality at harvest and during storage. J. Sci. Food Agric. 87:2409-15. DOI: https://doi.org/10.1002/jsfa.2905
Pii Y, Borruso L, Brusetti L, Crecchio C, Cesco S, Mimmo T, 2016. The interaction between iron nutrition, plant species and soil type shapes the rhizosphere microbiome. Plant Physiol. Biochem. 99:39-48. DOI: https://doi.org/10.1016/j.plaphy.2015.12.002
Porcel R, Zamarreño ÁM, García-Mina JM, Aroca R, 2014. Involvement of plant endogenous ABA in Bacillus megaterium PGPR activity in tomato plants. BMC Plant Biol. 14:1-12. DOI: https://doi.org/10.1186/1471-2229-14-36
Poudel R, Jumpponen A, Kennelly MM, Rivard CL, Gomez-Montano L, Garrett KA, 2019. Rootstocks shape the rhizobiome: rhizosphere and endosphere bacterial communities in the grafted tomato system. Appl. Env. Microbiol. 85:e01765-18.
Rounis V, Skarmoutsos K, Tsaniklidis G, Nikoloudakis N, Delis C, Karapanos I, Aivalakis G, 2015. Seeded and parthenocarpic cherry tomato fruits exhibit similar sucrose, glucose, and fructose levels, despite dissimilarities in UGPase and SPS gene expression and enzyme activity. J. Plant Growth Regul. 34:47-56.
Qu Q, Li Y, Zhang Z, Cui H, Zhao Q, Liu W, Qian H, 2021. Effects of S-metolachlor on wheat (Triticum aestivum L.) seedling root exudates and the rhizosphere microbiome. J. Haz. Mat. 411:125137.
Quinet M, Angosto T, Yuste-Lisbona FJ, Blanchard-Gros R, Bigot S, Martinez JP, Lutts S, 2019. Tomato fruit development and metabolism. Front. Plant Sci. 10:1554. DOI: https://doi.org/10.3389/fpls.2019.01554
Rodrigues BM, Souza BD, Nogueira RM, Santos MG, 2010. Tolerance to water deficit in young trees of jackfruit and sugar apple. Rev. Ciencia Agron. 41:245-52. DOI: https://doi.org/10.1590/S1806-66902010000200011
Sacco A, Greco B, Di Matteo A, De Stefano R, Barone A, 2013. Evaluation of tomato genetic resources for response to water deficit. Am. J. Plant Sci. 4:131. DOI: https://doi.org/10.4236/ajps.2013.412A3016
Sánchez-Rodríguez E, Rubio-Wilhelmi MM, Blasco B, Constán-Aguilar C, Romero L, Ruiz JM, 2011. Variation in the use efficiency of N under moderate water deficit in tomato plants (Solanum lycopersicum) differing in their tolerance to drought. Acta Physiol. Plant. 33:1861-65. DOI: https://doi.org/10.1007/s11738-011-0729-5
Sandrini M, Nerva L, Sillo F, Balestrini R, Chitarra W, Zampieri E, 2022. Abiotic stress and belowground microbiome: the potential of omics approaches. Int. J. Mol. Sci. 23:1091. DOI: https://doi.org/10.3390/ijms23031091
Santos-Medellín C, Liechty Z, Edwards J, Nguyen B, Huang B, Weimer BC, Sundaresan V, 2021. Prolonged drought imparts lasting compositional changes to the rice root microbiome. Nature Plants 7:1065-77.
Schlemper TR, Leite MF, Lucheta A, Shimels M, Bouwmeester HJ, van Veen JA, Kuramae EE, 2017. Rhizobacterial community structure differences among sorghum cultivars in different growth stages and soils. FEMS Microbiol. Ecol. 93. DOI: https://doi.org/10.1093/femsec/fix096
Singer E, Bonnette J, Kenaley SC, Woyke T, Juenger TE, 2019. Plant compartment and genetic variation drive microbiome composition in switchgrass roots. Env. Microbiol. Rep. 11:185-95. DOI: https://doi.org/10.1111/1758-2229.12727
Sorty AM, Meena KK, Choudhary K, Bitla UM, Minhas PS, Krishnani KK, 2016. Effect of plant growth promoting bacteria associated with halophytic weed (Psoralea corylifolia L) on germination and seedling growth of wheat under saline conditions. Appl. Biochem. Biotech.180:872-82.
Strasser RJ, Tsimilli-Michael M, Srivastava A, 2004. Analysis of the chlorophyll a fluorescence transient. In: GC, Papaqeorgiou, Govindjee (Eds.), Chlorophyll a fluorescence. Springer, Dordrecht, pp 321-362. DOI: https://doi.org/10.1007/978-1-4020-3218-9_12
Terry LA, Chope GA, Bordonaba JG, 2007. Effect of water deficit irrigation and inoculation with Botrytis cinerea on strawberry (Fragaria x ananassa) fruit quality. J. Agric. Food Chem. 55:10812-19.
Tahi H, Wahbi S, Wakrim R, Aganchich B, Serraj R, Centritto M, 2007. Water relations, photosynthesis, growth and water-use efficiency in tomato plants subjected to partial rootzone drying and regulated deficit irrigation. Plant Biosyst. 141:265-74. DOI: https://doi.org/10.1080/11263500701401927
The Tomato Genome Consortium, 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635-641. DOI: https://doi.org/10.1038/nature11119
Tiwari S, Singh P, Tiwari R, Meena KK, Yandigeri M, Singh DP, Arora DK, 2011. Salt-tolerant rhizobacteria-mediated induced tolerance in wheat (Triticum aestivum) and chemical diversity in rhizosphere enhance plant growth. Biol. Fert. Soils 47:907-16. DOI: https://doi.org/10.1007/s00374-011-0598-5
Tomato Genetics Resource Center, 2019. Available from: https://tgrc.ucdavis.edu/
Vardharajula S, Zulfikar Ali S, Grover M, Reddy G, Bandi V, 2011. Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J. Plant Interact. 6:1-14. DOI: https://doi.org/10.1080/17429145.2010.535178
Walters WA, Jin Z, Youngblut N, Wallace JG, Sutter J, Zhang W, Ley RE, 2018. Large-scale replicated field study of maize rhizosphere identifies heritable microbes. Proc. Natl. Acad. Sci. U. S. A. 115:7368-73. DOI: https://doi.org/10.1073/pnas.1800918115
Williams A, de Vries FT, 2020. Plant root exudation under drought: implications for ecosystem functioning. New Phytol. 225:1899-905. DOI: https://doi.org/10.1111/nph.16223
Yang J, Kloepper JW, Ryu CM, 2009. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1-4. DOI: https://doi.org/10.1016/j.tplants.2008.10.004
Yang Y, Tang N, Xian Z, Li Z, 2015. Two SnRK2 protein kinases genes play a negative regulatory role in the osmotic stress response in tomato. Plant Cell Tissue Organ Cult. 122:421-34. DOI: https://doi.org/10.1007/s11240-015-0779-2
Yasmin H, Bano A, Wilson NL, Nosheen A, Naz R, Hassan MN, Kennedy I, 2022. Drought‐tolerant Pseudomonas sp. showed differential expression of stress‐responsive genes and induced drought tolerance in Arabidopsis thaliana. Physiol. Plant. 174:e13497. DOI: https://doi.org/10.1111/ppl.13497
Zhang J, Schurr U, Davies WJ, 1987. Control of stomatal behaviour by abscisic acid which apparently originates in the roots. J. Exp. Bot. 38:1174-81. DOI: https://doi.org/10.1093/jxb/38.7.1174
Zhang L, Chen W, Jiang Q, Fei Z, Xiao M, 2020. Genome analysis of plant growth-promoting rhizobacterium Pseudomonas chlororaphis subsp. aurantiaca JD37 and insights from comparasion of genomics with three Pseudomonas strains. Microbiol. Res. 237:126483. DOI: https://doi.org/10.1016/j.micres.2020.126483
Zhang X, Myrold DD, Shi L, Kuzyakov Y, Dai H, Hoang DTT, Razavi BS, 2021. Resistance of microbial community and its functional sensitivity in the rhizosphere hotspots to drought. Soil Biol. Biochem. 161:108360.

How to Cite

Sillo, F., Marino, G., Franchi, E., Haworth, M., Zampieri, E., Pietrini, I., Fusini, D., Mennone, C., Centritto, M., & Balestrini, R. (2022). Impact of irrigation water deficit on two tomato genotypes grown under open field conditions: From the root-associated microbiota to the stress responses. Italian Journal of Agronomy, 17(3). https://doi.org/10.4081/ija.2022.2130