Abstract
Research on seed microbiota gained much attention as it constitutes a primary inoculum for plants and supports their growth, fitness and productivity. This research aimed to explore the uniqueness and impact of culturable seed-endophytes on a widely cultivated rice host plant. In this report, we present the nature of seed-borne endophytic bacteria from cultivated rice (Oryza sativa L.) variety Ajinkya-1040 and their crucial roles in plant growth promotion and biocontrol. We report characters of five culturable rice-seed-borne endophytic bacteria Bacillus sp. RSE01, Citrobacter sp. RSE02, Citrobacter sp. RSE03, Flavobacterium sp. RSE04, and Pantoea sp. RSE05 which are not reported before from seeds of rice cultivars. These isolates showed plant growth-promoting activities by producing phytohormones, siderophores, ammonia, hydrogen cyanide (HCN), solubilizing minerals or by fixing N2 and showed antagonistic effects against various fungal pathogens of rice. Among the isolates, Citrobacter sp. RSE02 showed highest IAA (34.51 ± 0.23 µg/mL), GA (55.43 ± 0.29 µg/mL), siderophore (95.68%) and HCN production ability. Whereas, Pantoea sp. RSE05 showed the highest efficacy for phosphate (83.19 ± 1.45), potassium solubilization (82.27 ± 0.6 µg/mL) as well as ammonia-producing efficiency. Furthermore, these seed endophytes can readily migrate from the seeds to the roots and shoots of the germinated seedlings. Seedlings fortified with the endophytic culture showed an overall increase in root and shoot length (1.5-fold and 2-fold, respectively). Most of the isolates inhibit the mycelial growth of selected fungal pathogens of rice. These results suggest that the isolated seed endophytes can potentially be used to assist plant growth and development and help host plant to fight against fungal phytopathogens for eco-friendly and sustainable agriculture.
Graphical Abstract
Highlights
-
1.
Rice seed endophytes transmit into the seedling upon seed germination.
-
2.
Rice seed endophytes help in seed germination.
-
3.
Rice seed endophytes promote the growth of rice plants.
-
4.
The seed endophytes are biocontrol agents as they inhibit fungal rice pathogens.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ariffin H, Abdullah N, Umi Kalsom MS, Shirai Y, Hassan MA (2006) Production and characterization of cellulase by Bacillus pumilus EB3. Int J Eng Technol 3:47–53
Borah M, Das S, Bora SS, Boro RC, Barooah M (2021) Comparative assessment of multi-trait plant growth-promoting endophytes associated with cultivated and wild Oryza germplasm of Assam, India. Arch Microbiol 203:2007–2028. https://doi.org/10.1007/s00203-020-02153-x
Brader G, Compant S, Mitter B, Trognitz F, Sessitsch A (2014) Metabolic potential of endophytic bacteria. Curr Opin Biotechnol 27:30–37. doi: https://doi.org/10.1016/j.copbio.2013.09.012
Cao L, Gao Y, Yu J, Niu S, Zeng J, Yao Q, Zhu Y (2021) Streptomyces hygroscopicus OsiSh-2-induced mitigation of Fe deficiency in rice plants. Plant Physiol Biochem 158:275–283. doi: https://doi.org/10.1016/j.plaphy.2020.11.013
Chauhan A, Guleria S, Balgir PP, Walia A, Mahajan R, Mehta P, Shirkot CK (2017) Tricalcium phosphate solubilization and nitrogen fixation by newly isolated Aneurinibacillus aneurinilyticus CKMV1 from rhizosphere of Valeriana jatamansi and its growth promotional effect. Braz J Microbiol 48:294–304. doi: https://doi.org/10.1016/j.bjm.2016.12.001
De Silva NI, Brooks S, Lumyong S, Hyde KD (2019) Use of endophytes as biocontrol agents. Fungal Biol Rev 33:133–148. https://doi.org/10.1016/j.fbr.2018.10.001
Dean RA, Talbot NJ, Ebbole DJ, Farman ML, Mitchell TK, Orbach MJ, Birren BW (2005) The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434:980–986. https://doi.org/10.1038/nature03449
del Ángel EC, Hernández FD, Fuentes YMO, Morales GG, Reyes FC, Tucuch FM (2017) Endophytic bacteria controlling Fusarium oxysporum and Rhizoctonia solani in Solanum tuberosum. EJPAS Vol, 5(1)
Devi R, Thakur R (2018) Screening and identification of bacteria for plant growth promoting traits from termite mound soil. J Pharmacogn Phytochem 7:1681–1686
Di Benedetto NA, Campaniello D, Bevilacqua A, Cataldi MP, Sinigaglia M, Flagella Z, Corbo MR (2019) Isolation, screening, and characterization of plant-growth-promoting bacteria from durum wheat rhizosphere to improve N and P nutrient use efficiency. Microorganisms 7:541. https://doi.org/10.3390/microorganisms7110541
Döbereiner J (1989) Isolation and identification of root associated diazotrophs. Nitrogen fixation with non-legumes. Springer, Dordrecht, pp 103–108. doi: https://doi.org/10.1007/BF02226800
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. PNAS 112(8):911–920. https://doi.org/10.1073/pnas.1414592112
Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato YI, Morisaki H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46:617–629. https://doi.org/10.1080/00380768.2000.10409127
Gaur AC (1990) Phosphate solubilizing micro-organisms as biofertilizer. Omega scientific publishers
Gond SK, Bergen MS, Torres MS, White JF Jr (2015) Endophytic Bacillus spp. produce antifungal lipopeptides and induce host defence gene expression in maize. Microbiol Res 172:79–87. https://doi.org/10.1016/j.micres.2014.11.004
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192. https://dx.doi.org/10.1104%2Fpp.26.1.192
Gupta S, Pandey S (2019) ACC deaminase producing bacteria with multifarious plant growth promoting traits alleviates salinity stress in French bean (Phaseolus vulgaris) plants. Front Microbiol 10:1506. https://doi.org/10.3389/fmicb.2019.01506
Hardoim PR, Hardoim CC, Van Overbeek LS, Van Elsas JD (2012) Dynamics of seed-borne rice endophytes on early plant growth stages. PLoS ONE 7:e30438. https://doi.org/10.1371/journal.pone.0030438
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320. https://doi.org/10.1128/MMBR.00050-14
Hu X, Chen J, Guo J (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22:983–990. https://doi.org/10.1007/s11274-006-9144-2
Jana SK, Islam MM, Mandal S (2022) Endophytic Microbiota of Rice and Their Collective Impact on Host Fitness. Curr Microbiol 79:1–10. https://doi.org/10.1007/s00284-021-02737-w
Kaur G, Sharma P, Chhabra D, Chand K, Mangat GS (2017) Exploitation of endophytic Pseudomonas sp. for plant growth promotion and colonization in rice. J Appl Nat Sci 9:1310–1316. https://doi.org/10.31018/jans.v9i3.1359
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Kumar K, Pal G, Verma A, Verma SK (2020) Seed inhabiting bacterial endophytes of finger millet (Eleusine coracana L.) promote seedling growth and development, and protect from fungal disease. S Afr J Bot 134:91–98. https://doi.org/10.1016/j.sajb.2020.03.032
Kumar K, Verma A, Pal G, Anubha A, White JF, Verma SK (2021) Seed endophytic bacteria of pearl millet (Pennisetum glaucum L.) promote seedling development and defend against a fungal phytopathogen. Front Microbiol 3660. DOI: https://doi.org/10.3389/fmicb.2021.774293
Ladha JK, Reddy PM (2003) Nitrogen fixation in rice systems: state of knowledge and future prospects. Plant Soil 252:151–167. https://doi.org/10.1023/A:1024175307238
Louden BC, Haarmann D, Lynne AM (2011) Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ 12:51–53. https://doi.org/10.1128/jmbe.v12i1.249
Maiti PK, Das S, Sahoo P, Mandal S (2020) Streptomyces sp SM01 isolated from Indian soil produces a novel antibiotic picolinamycin effective against multi drug resistant bacterial strains. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-66984-w
Maiti PK, Mandal S (2019) Majority of actinobacterial strains isolated from Kashmir Himalaya soil are rich source of antimicrobials and industrially important biomolecules. Adv Microbiol 9:220. DOI:https://doi.org/10.4236/aim.2019.93016
Marmur J (1961) A procedure for the isolation of deoxyribonucleic acid from micro-organisms. J Mol Biol 3:208–IN1. https://doi.org/10.1016/S0022-2836(61)80047-8
Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56. https://doi.org/10.1007/s002840010259
Miliute I, Buzaite O, Baniulis D, Stanys V (2015) Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agric 102:465–478. doi:https://doi.org/10.13080/z-a.2015.102.060
Mir MI, Hameeda B, Quadriya H, Kumar BK, Ilyas N, Zuan ATK, Sayyed RZ (2021) Multifarious Indigenous Diazotrophic Rhizobacteria of Rice (Oryza sativa L.) Rhizosphere and Their Effect on Plant Growth Promotion. Front Nutr 8. https://doi.org/10.3389/fnut.2021.781764
Ríos-Ruiz WF, Torres-Chávez EE, Torres-Delgado J, Rojas-García JC, Bedmar EJ, Valdez-Nuñez RA (2020) Inoculation of bacterial consortium increases rice yield (Oryza sativa L.) reducing applications of nitrogen fertilizer in San Martin region, Peru. Rhizosphere 14:100200. https://doi.org/10.1016/j.rhisph.2020.100200
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sharma S, Sharma A, Kaur M (2018) Extraction and evaluation of gibberellic acid from Pseudomonas sp.: Plant growth promoting rhizobacteria. J Pharmacogn Phytochem 7:2790–2795
Sharma SKMP, Ramesh A, Joshi OP (2011) Characterization of zinc-solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds. https://doi.org/10.4014/jmb.1106.05063
Shridhar BS (2012) Nitrogen fixing microorganisms. Int J Microbiol Res 3:46–52. https://doi.org/10.5829/idosi.ijmr.2012.3.161103
Srinivasulu B, Prakasham RS, Jetty A, Srinivas S, Ellaiah P, Ramakrishna SV (2002) Neomycin production with free and immobilized cells of Streptomyces marinensis in an airlift reactor. Process Biochem 38:593–598. https://doi.org/10.1016/S0032-9592(02)00182-6
Sunitha VH, Devi DN, Srinivas C (2013) Extracellular enzymatic activity of endophytic fungal strains isolated from medicinal plants. World J Agric Sci 9:01–09. DOI: https://doi.org/10.5829/idosi.wjas.2013.9.1.72148
Swamy MK, Akhtar MS, Sinniah UR (2016) Response of PGPR and AM fungi toward growth and secondary metabolite production in medicinal and aromatic plants. In Plant, soil and microbes pp. 145–168. Springer, Cham. https://doi.org/10.1007/978-3-319-29573-2_7
Tan KZ, Radziah O, Halimi MS, Khairuddin AR, Habib SH, Shamsuddin ZH (2014) Isolation and characterization of rhizobia and plant growth-promoting rhizobacteria and their effects on growth of rice seedlings. Am J Agric Biol Sci 9:342–360. doi: https://doi.org/10.3844/ajabssp.2014.342.360
Truyens S, Weyens N, Cuypers A, Vangronsveld J (2015) Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Rep 7:40–50. https://doi.org/10.1111/1758-2229.12181
Turner S, Pryer KM, Miao VP, Palmer JD (1999) Investigating deep phylogenetic relationships among cyanobacteria and plastids by small subunit rRNA. Seq Anal J Eukaryot 46:327–338. https://doi.org/10.1111/j.1550-7408.1999.tb04612.x
Verma SK, Kingsley K, Irizarry I, Bergen M, Kharwar RN, White JF Jr (2017) Seed-vectored endophytic bacteria modulate development of rice seedlings. J Appl Microbiol 122:1680–1691. https://doi.org/10.1111/jam.13463
Verma SK, Sahu PK, Kumar K, Pal G, Gond SK, Kharwar RN, White JF (2021) Endophyte roles in nutrient acquisition, root system architecture development and oxidative stress tolerance. J Appl Microbiol 131:2161–2177. https://doi.org/10.1111/jam.15111
Verma SK, White JF (2018) Indigenous endophytic seed bacteria promote seedling development and defend against fungal disease in browntop millet (Urochloa ramosa L.). J Appl Microbiol 124:764–778. https://doi.org/10.3390/microorganisms6010021
Walitang DI, Kim K, Madhaiyan M, Kim YK, Kang Y, Sa T (2017) Characterizing endophytic competence and plant growth promotion of bacterial endophytes inhabiting the seed endosphere of Rice. BMC Microbiol 17:1–13. https://doi.org/10.1186/s12866-017-1117-0
Welbaum GE, Sturz AV, Dong Z, Nowak J (2004) Managing soil microorganisms to improve productivity of agro-ecosystems. CRC Crit Rev Plant Sci 23:175–193. https://doi.org/10.1080/07352680490433295
Whipps JM (1997) Developments in the biological control of soil-borne plant pathogens. Adv Bot Res 26:1–134. https://doi.org/10.1016/S0065-2296(08)60119-6
Yadav R, Singh AV, Joshi S, Kumar M (2015) Antifungal and enzyme activity of endophytic fungi isolated from Ocimum sanctum and Aloe vera. Afr J Microbiol Res 9:1783–1788. https://doi.org/10.5897/AJMR2015.7451
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. IJSEM 67:1613. https://dx.doi.org/10.1099%2Fijsem.0.001755
Yu YY, Jiang CH, Wang C, Chen LJ, Li HY, Xu Q, Guo JH (2017) An improved strategy for stable biocontrol agents selecting to control rice sheath blight caused by Rhizoctonia solani. Microbiol Res 203:1–9. https://doi.org/10.1016/j.micres.2017.05.006
Acknowledgements
We are grateful to Dr. Prithidipa Sahoo, Visva-Bharati University for her generous help to critically proofread the manuscript. M.M.I. thankfully acknowledge the financial support in form of fellowship (UGC Ref No-712/CSIR-UGC NET DEC.2017) by the University Grant Commission, New Delhi, India.
Funding
There is no financial support for this research.
Author information
Authors and Affiliations
Contributions
SKJ conceptualize the research, design the methodology, analyse the data, and prepare the manuscript; MMI helped in characterization of the isolates; SH helped in statistical analysis of the data; SM conceptualize and supervise the research, help acquisition of the financial support for the research and edit the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest.
Ethical approval
The research is not associated with any prior ethical approval.
Consent of publication
The data used for the manuscript is original and does not require any consent from third party for publication.
Additional information
Communicated by Xiue Wang.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Jana, S.K., Islam, M.M., Hore, S. et al. Rice seed endophytes transmit into the plant seedling, promote plant growth and inhibit fungal phytopathogens. Plant Growth Regul 99, 373–388 (2023). https://doi.org/10.1007/s10725-022-00914-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-022-00914-w