Various signaling interactions of IAA.
Abstract
Phytohormones play a fundamental role in the development of plants. Among various phytohormones produced by the plants, Auxins act as a master hormone that plays a major role during plant development and differentiation through cell division. Besides plants, many rhizospheric microorganisms are also capable of producing auxins specifically indole-3-acetic acid (IAA), that act as signaling molecules for the regulation of gene expressions in plants. However, bacterial IAA is majorly linked with the modulation of plant roots architecture and developing positive plant-microbe interactions. Bacterial auxin modifies root morphology by enhancing root length, forming adventitious root and root hair, thereby, increasing surface area for water and nutrient absorption affecting various aspects of plant biology in a number of ways. Bacteria mostly utilize tryptophan, present in plant root exudates, to synthesize IAA that eventually helps bacteria to colonize roots by establishing beneficial associations with plant roots. Auxins also stimulate the formation of exopolysaccharides and biofilms that help bacterial root colonization. Auxins have given the survival benefit to rhizobacteria that make them more competent to establish symbiotic interaction with plants. Synergistic and antagonistic interactions of auxins (both interkingdom and Intrakingdom) with other phytohormones play a key role in plant development and growth improvement.
Keywords
- Auxins
- bacterial IAA
- phytostimulation
- Indole-3-acetamide
- Tryptophan
1. Introduction
Auxins are mainly synthesized in meristematic tissues and transported to other plant parts. Auxins play a critical role in controlling various processes during growth and development across variable environmental conditions, even at lower concentrations, these can modulate gene expression by interacting with specific proteins involved in the transcription process [1]. The plant rhizosphere is enriched with a diversity of microflora that directly contributes to their growth. The rhizosphere microbiota has the ability to produce phytohormones as a signaling molecule for inter and intraspecies communications. The synthesis and release of auxins establish a mutualistic or morbific link between organisms. Indole-3-acetic acid (IAA) is a widely produced rhizobacterial signaling phytohormone. Primarily, auxin controls various physiological processes, such as cell division, elongation, phototactic, and geotactic responses, in plants [2]. Thus, in nature, plants are receiving endogenous and exogenous signals simultaneously influencing their developmental patterns. Endogenous auxin can either be free (active auxin) or act as storage intermediates as conjugated compounds with amino acids and sugars [3]. Since higher auxin levels cause inhibitory effects, therefore, homeostasis and coordination of auxin signaling within plants and their surroundings are necessary for their regular growth and development. Endogenous auxin levels suggest the type of interactions between plant and rhizobacteria. Generally, three possible plant-bacterial IAA associations have been stated so far, first, due to direct transfer of bacterial IAA genes into host cell; second, due to bacteria living and releasing IAA within plant tissues and lastly, due to bacteria colonizing plant surfaces and producing IAA [4]. The first two associations usually result from pathogenic interactions. The knowledge of deciphering these signals and their outcomes is critical for the development of strategies for sustainable agricultural practices. Thus, the present chapter highlights the significant role of bacterial IAA as a potent microbial signaling molecule regarding beneficial plant-rhizobacterial interactions which are important for ecological resilience and sustainability.
2. Biosynthetic pathways of auxins
Conferring to key intermediate compounds, five different pathways for IAA synthesis have been reported in bacteria using tryptophan precursors [5]. Rhizobacteria use tryptophane either from plant root exudates or synthesize through chorismate precursor using trp gene by shikimate pathway [6, 7]. Rhizobia are an example of rhizobacteria that utilize host tryptophan for IAA synthesis [8]. Zhang
3. IAA – Signaling molecule
Intrakingdom Signaling
Auxins modulate the gene expression making it inter and intrakingdom communicating chemical messenger and quorum-sensing molecule. Scott
Interkingdom Signaling
Signal exchange between plant and rhizospheric bacteria occurs through the release of root exudates [34]. This signaling is key for developing and determining the nature of plant-bacterial interactions (symbiotic or pathogenic). PGPR colonization is the result of these signaling activities. Besides IAA synthesis, many rhizobacterial species have the ability to degrade IAA. This IAA degrading ability has given the advantage to bacteria for rhizospheric colonization and manipulating plant physiology for their survival. However, the mechanism of how IAA degradation is beneficial for plants and bacteria is not well studied and needed to be explored. Zuniga
The role of bacterially produced IAA has been very significant in plant growth promotion and has been investigated by various researchers. Ahmed and Hasnain [19] studied auxin production ability and potential plant growth promotional activity of two gram-positive
Source | Plant | Effects | Cross-signaling mechanism | Reference |
---|---|---|---|---|
Root architecture modified by inhibition of primary root elongation and promotion of lateral root and root hair | Auxins interacting with volatile organic compounds | [48] | ||
Soybean | Enhanced shoot growth and improved dry mass | Auxins interacting with ACC deaminase production | [49] | |
Increased shoot and root dry weight, and shoot length | Auxin + solubilized phosphate interaction | [50] | ||
Bamboo seedlings | Enhance chlorophyll content | Auxin trigger the chlorophyll related enzymes | [51] | |
Increased the expression of TARGET OF RAPAMYCIN (TOR) in shoot and root apexes and induce phosphorylation | Auxin + TOR signaling | [52] | ||
Increased shoot and root biomass, lateral roots number per plant, and root hair formation but no effect on primary root length | Induction of auxin signaling | [47] | ||
Maize roots | Enhanced root development and reduced lipid peroxidation | Induction of auxin signaling | [53] |
4. Conclusions
Auxin is a key phytohormone controlling the whole physiology of plants by interacting and regulating other phytohormones as well. Besides plants, various rhizobacteria have the ability to produce auxins. Various auxin biosynthetic pathways act simultaneously to regulate auxin formation. These pathways in plants and bacteria are highly similar, however, the tryptophan side chain oxidase pathway is the mechanism found only in bacteria. The main precursor for auxin synthesis is tryptophan, however, tryptophan-independent routes are also present but these routes are not well described and need to be studied. Auxin besides controlling plant growth and development, also affects various regulatory processes in bacteria as well, making inter and intrakingdom cross-signaling interactions. In bacteria, auxin primarily supports bacterial survival by strengthening their stress tolerance mechanism and also enhancing colonizing ability. This also helps in bacterial rhizospheric competence making them more adaptive to the environment. As an interkingdom signaling molecule, auxins interact with various plant signaling mechanisms and coordinate various plant growth processes. Auxins directly affect plant root architecture helping plants for enhanced nutrient and water uptake even under various stress conditions. Plants under optimum auxin levels showed enhanced and prolonged root systems but higher levels of auxin do not increase root length instead initiate the formation of lateral roots and root hair. However, very low auxin levels do not show any effect on root growth. Thus, auxins exert a significant impact (either directly or indirectly) on the healthy development and growth of the plants in a coordinated manner.
References
- 1.
Kan J, Fang R, Jia Y. Interkingdom signaling in plant-microbe interactions. Science China Life Sciences. 2017; 60 (8):785-796. DOI: 10.1007/s11427-017-9092-3 - 2.
Zhao Y. Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biology. 2010; 61 :49-64. DOI: 10.1146/annurev-arplant-042809-112308 - 3.
Ludwig-Müller J. Auxin conjugates: Their role for plant development and in the evolution of land plants. Journal of Experimental Botany. 2011; 62 (6):1757-1773. DOI: 10.1093/jxb/erq412 - 4.
Patten CL, Glick BR. Bacterial biosynthesis of indole-3-acetic acid. Canadian Journal of Microbiology. 1996; 42 (3):207-220. DOI: 10.1139/M96-032 - 5.
Spaepen S, Vanderleyden J, Remans R. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiology Reviews. 2007; 31 (4):425-448. DOI: 10.1111/J.1574-6976.2007.00072.x - 6.
Kamilova F, Validov S, Azarova T, Mulders I, Lugtenberg B. Enrichment for enhanced competitive plant root tip colonizers selects for a new class of biocontrol bacteria. Environmental Microbiology. 2005; 7 (11):1809-1817. DOI: 10.1111/j.1462-2920.2005.00889.x - 7.
Spaepen S, Vanderleyden J. Auxin and plant-microbe interactions. Cold Spring Harbor Perspectives in Biology. 2011; 3 (4):1-15. DOI: 10.1101/cshperspect. a001438 - 8.
Kefford NP, Brockwell J, Zwar JA. The symbiotic synthesis of auxin by legumes and nodule bacteria and its role in nodule development. Australian Journal of Biological Sciences. 1960; 13 (4):456-467. DOI: 10.1071/BI9600456 - 9.
Zhang P, Jin T, Sahu SK, Xu J, Shi Q , Liu H, et al. The distribution of tryptophan-dependent indole-3-acetic acid synthesis pathways in bacteria unraveled by large-scale genomic analysis. Molecules. 2019; 24 (7). DOI: 10.3390/molecules24071411 - 10.
Brown ME, Burlingham LSK. Production of plant growth substances by Azotobacter chroococcum. J Gen Microbial. 1968; 53 (1):135-144. DOI: 10.1099/00221287-53-1-135 - 11.
Merzaeva DV, Shirokikh IG. The production of auxins by the endophytic bacteria of winter rye. Applied Biochemistry and Microbiology. 2010; 46 (1):44-50. DOI: 10.1134/S0003683810010072 - 12.
Kiyohara S, Honda H, Shimizu N, Ejima C, Hamasaki R, Sawa S. Tryptophan auxotroph mutants suppress the superroot 2 phenotypes, modulating IAA biosynthesis in Arabidopsis. Plant Signaling & Behavior. 2011; 6 (9):1351-1355. DOI: 10.4161/psb.6.9.16321 - 13.
Prinsen E, Costacura A, Michiels K, Vanderleyden J, Van Onckelen H. Azospirillum brasilense indole-3-acetic acid biosynthesis: Evidence for a non-tryptophan dependent pathway. Molecular Plant-Microbe Interactions. 1993;6 (5):609-615. DOI: - 14.
Li M, Guo R, Yu F, Chen X, Zhao H, Li H, et al. Indole-3-acetic acid biosynthesis pathways in the plant-beneficial bacterium Arthrobacter pascens ZZ21. International Journal of Molecular Sciences. 2018;19 (2):1-15. DOI: 10.3390/ijms19020443 - 15.
Ahmad E, Sharma SK, Sharma PK. Deciphering operation of tryptophan-independent pathway in high indole-3-acetic acid (IAA) producing Micrococcus aloeverae DCB-20. FEMS Microbiology Letters. 2020; 24 :fnaa190. DOI: 10.1093/femsle/fnaa190 - 16.
Wagi S, Ahmed A. Bacillus spp.: Potent microfactories of bacterial IAA. Peer J. 2019; 7 :e7258. DOI: 10.7717/peerj.7258 - 17.
Ahmed A, Hasnain S. Extraction and evaluation of indole acetic acid from indigenous auxin-producing rhizosphere bacteria. J. Anim. Plant Sci. 2020; 4 :1024-1036. DOI: 10.36899/JAPS.2020.4.0117 - 18.
Suliasih WS. Isolation of Indole Acetic Acid (IAA) producing Bacillus siamensis from peat and optimization of the culture conditions for maximum IAA production. In IOP Conference Series: Earth and Environmental Science. 2020; 572 (1):1-12. DOI: 10.1088/1755-1315/572/1/012025 - 19.
Ahmed A, Hasnain S. Auxin-producing Bacillus sp.: Auxin quantification and effect on the growth of Solanum tuberosum. Pure and Applied Chemistry. 2010; 1 :313-319. DOI: 10.1351/PAC-CON-09-02-06 - 20.
Vande Broek A, Gysegom P, Ona O, Hendrickx N, Prinsen E, Van Impe J, et al. Transcriptional analysis of the Azospirillum brasilense indole-3-pyruvate decarboxylase gene and identification of a cis-acting sequence involved in auxin responsive expression. Molecular Plant-Microbe Interactions. 2005; 18 (4):311-323. DOI: 10.1094/MPMI-18-0311 - 21.
Patten CL, Glick BR. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Applied and Environmental Microbiology. 2002; 68 (8):3795-3801. DOI: 10.1128/AEM.68.8.3795-3801.2002 - 22.
Kang BR, Yang K, Y, Cho B. H, Han T. H, Kim I. S, Lee M. C, Anderson A. J, Kim Y. C., Production of indole-3- acetic acid in the plant-beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase Gac S. Current Microbiol. 2006; 52 :473-476. DOI: 10.1007/s00284-005-0427-x - 23.
Ryu RJ, Patten CL. Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J Bacteriology. 2008; 190 (21):7200-7208. DOI: 109.1128/JB.00804-08 - 24.
Keswani C, Singh SP, Cueto L, García-Estrada C, Mezaache-Aichour S, Glare TR, et al. Auxins of microbial origin and their use in agriculture. Applied Microbiology and Biotechnology. 2020; 140 :1-17. DOI: 10.1007/s00253-020-10890-8 - 25.
Persello-Cartieaux F, Nussaume L, Robaglia C. Tales from the underground: molecular plant–rhizobacteria interactions. Plant Cell Environment. 2003; 26 (2):189-199. DOI: 10.1046/j.1365-3040.2003. 00956.x - 26.
Scott JC, Greenhut IV, Leveau JHJ. Functional characterization of the bacterial iac genes for degradation of the plant hormone indole 3-acetic acid. Journal of Chemical Ecology. 2013; 39 :942-951. DOI: 10.1007/s10886-013-0324-x - 27.
Patten CL, Blakney AJC, Coulson TJD. Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Critical Reviews in Microbiology. 2013; 39 (4):395-415. DOI: 10.3109/1040841X.2012.716819 - 28.
Kim JI, Murphy AS, Baek D, Lee S, Yun D, Bressan RA, et al. L (2011a) YUCCA6 over-expression demonstrates auxin function in delaying leaf senescence in Arabidopsis thaliana. Journal of Experimental Botany. 2011; 62 (11):3981-3992. DOI: 10.1093/jxb/err094 - 29.
Bianco C, Imperlini E, Defez R. Legumes like more IAA. Plant Signaling & Behavior. 2009; 4 :763-765. DOI: 10.4161/psb.4.8.9166 - 30.
Donati AJ, Lee HI, Leveau JHJ, Chang WS. Effects of indole-3- acetic acid on the transcriptional activities and stress tolerance of Bradyrhizobium japonicum. PLoS One. 2013; 8 :1-11. DOI: 10.1371/journal.pone.0076559 - 31.
Molina R, Rivera D, Mora V, López G, Rosas S, Spaepen S, et al. Regulation of IAA biosynthesis in Azospirillum brasilense under environmental stress conditions. Current Microbiology. 2018; 75 (10):1408-1418. DOI: 10.1007/s00284-018-1537-6 - 32.
Van Puyvelde S, Cloots L, Engelen K, Das F, Marchal K, Vanderleyden J, et al. Transcriptome analysis of the rhizosphere bacterium Azospirillum brasilense reveals an extensive auxin response. Microb Ecology. 2011; 61 :723-728. DOI: 10.1007/s00248-011-9819-6 - 33.
Yang S, Zhang Q , Guo J, Charkowski AO, Glick B. R, Ibekwe A. M. et al . Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl Environ Microbiology, 2007; 73(4):1079– 1088. DOI:10.1128/AEM.01770-06 - 34.
Phour M, Sehrawat A, Sindhu SS, Glick BR. Interkingdom signaling in plant-rhizomicrobiome interactions for sustainable agriculture. Microbiological Research. 2020; 241 . DOI: 10.1016/j.micres.2020.126589 - 35.
Zuniga A, Poupin MJ, Donoso R, Ledger T, Guiliani N. Quorum sensing and indole-3-acetic acid degradation play a role in colonization and plant growth promotion of Arabidopsis thaliana by Burkholderia phytofirmans PsJN. Molecular Plant-Microbe Interactions. 2013; 26 (5):546-553. DOI: 10.1094/MPMI-10-12-0241-R - 36.
Sukumar P, Legue V, Vayssieres A, Martin F, Tuskan GA, Kalluri UC. Involvement of auxin pathways in modulating root architecture during beneficial plant–microorganism interactions. Plant, Cell & Environment. 2013; 36 (5):909-919. DOI: 10.1111/pce.12036 - 37.
Ahmed A, Hasnain S. Auxins as one of the factors of plant growth improvement by plant growth promoting rhizobacteria. Polish Journal of Microbiology. 2014; 3 :261-266 - 38.
Ludwig-Müller J. Auxin and the interaction between plants and microorganisms. Auxin and its role in plant development. 2014:413-434. DOI: 10.1007/978-3-7091-1526-8_18 - 39.
Duca DR, Glick BR. Indole-3-acetic acid biosynthesis and its regulation in plant-associated bacteria. Applied Microbiology and Biotechnology. 2020:1-13. DOI: 10.1007/s00253-020-10869-5 - 40.
Mathesius U. Auxin: at the root of nodule development? Functional Plant Biology. 2008; 35 :651-668. DOI: 10.1071/FP08177 - 41.
Theunis M. IAA biosynthesis in rhizobia its potential role in symbiosis (thesis). Universiteit Antwerpen, Antwerp, Belgium; 2005 - 42.
Huo X, Schnabel E, Hughes K, Frugoli J. RNAi phenotypes and the localization of a protein: GUS fusion imply a role for Medicago truncatula PIN genes in nodulation. J Plant Growth Reg. 2006; 25 :156-165. DOI: 10.1007/s00344-005-0106-y - 43.
Glick BR. Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiological Research. 2013; 169 (1):30-39. DOI: 10.1016/j.micres.2013.09.009.0 - 44.
Fatima H, Ahmed A. Indole-3-acetic acid synthesizing chromium-resistant bacteria can mitigate chromium toxicity in Helianthus annuus L. Plant, Soil and Environ. 2020; 66 (5):216-221. DOI: 10.17221/581/2019-PSE - 45.
Ghosh A, Pramanik K, Bhattacharya S, Mondal S, Ghosh SK, Ghosh PK, et al. Abatement of arsenic-induced phytotoxic effects in rice seedlings by an arsenic-resistant Pantoea dispersa strain. Environmental Science and Pollution Research. 2021; 28 (17):1-17. DOI: 10.1007/s11356-020-11816-7 - 46.
Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moenne-Loccoz Y, Muller D, et al. Plant growth-promoting rhizobacteria and root system functioning. Frontiers in Plant Science. 2013; 4 :356. DOI: 10.3389/fpls.2013.00356 - 47.
Ortiz-Castro R, Campos-García J, López-Bucio J. Pseudomonas putida and Pseudomonas fluorescens influence Arabidopsis root system architecture through an auxin response mediated by bioactive cyclodipeptides. Journal of Plant Growth Reg. 2020; 39 (1):254-265. DOI: 10.1007/s00344-019-09979-w - 48.
Chu TN, Bui LV, Hoang MTT. Pseudomonas PS01 isolated from maize rhizosphere alters root system architecture and promotes plant growth. Microorganisms. 2020; 8 (4):471. DOI: 10.3390/microorganisms8040471 - 49.
Horstmann JL, Dias MP, Ortolan F, Medina-Silva R, Astarita LV, Santarém ER, et al. CLV45 from Fabaceae rhizosphere benefits growth of soybean plants. Brazilian Journal of Microbiology. 2020; 51 (4):1861-1871. DOI: 10.1007/s42770-020-00301-5 - 50.
Lebrazi S, Niehaus K, Bednarz H, Fadil M, Chraibi M, Fikri-Benbrahim K. Screening and optimization of indole-3-acetic acid production and phosphate solubilization by rhizobacterial strains isolated from Acacia cyanophylla root nodules and their effects on its plant growth. Journal of Genetic Engineering and Biotechnology. 2020; 18 (1):1-12. DOI: 10.1186/s43141-020-00090-2 - 51.
Maya KCB, Gauchan DP, Khanal SN, Chimouriya S, Lamichhane J. Extraction of Indole-3-acetic Acid from Plant Growth Promoting Rhizobacteria of Bamboo Rhizosphere and Its Effect on Biosynthesis of Chlorophyll in Bamboo Seedlings. Indian Journal of Agricultural Research. 2020; 54 (6):1-7. DOI: 10.18805/IJARe.A-5578 - 52.
Méndez-Gómez M, Castro-Mercado E, Peña-Uribe CA, Reyes-de la Cruz H, López-Bucio J, García-Pineda E. TARGET OF RAPAMYCIN signaling plays a role in Arabidopsis growth promotion by Azospirillum brasilense Sp245. Plant Science. 2020; 293 (110416). DOI: 10.1016/j.plantsci.2020.110416 - 53.
Zerrouk IZ, Rahmoune B, Auer S, Rößler S, Lin T, Baluska F, et al. Growth and aluminum tolerance of maize roots mediated by auxin-and cytokinin-producing Bacillus toyonensis requires polar auxin transport. Environmental and Experimental Botany. 2020; 176 :104064 - 54.
Jochum MD, McWilliams KL, Borrego EJ, Kolomiets MV, Niu G, Pierson EA, et al. Bioprospecting plant growth-promoting rhizobacteria that mitigate drought stress in grasses. Frontiers in Microbiology. 2019; 10 :2106. DOI: 10.3389/fmicb.2019.02106 - 55.
Batista BD, Dourado MN, Figueredo EF, Hortencio RO, Marques JPR, Piotto FA, et al. C., The auxin-producing Bacillus thuringiensis RZ2MS9 promotes the growth and modifies the root architecture of tomato (Solanum lycopersicum cv. Micro-Tom). Archives of Microbiology. 2021; 23 :3869-3882 - 56.
Oliveira DAD, Ferreira SDC, Carrera DLR, Serrao CP, Callegari DM, Barros NLF, et al. Characterization of Pseudomonas bacteria of Piper tuberculatum regarding the production of potentially bio-stimulating compounds for plant growth. Acta Amazonica. 2021; 51 :10-19