Cell division and turgor mediate enhanced plant growth in Arabidopsis plants treated with the bacterial signalling molecule lumichrome
Transcriptomic analysis indicates that the bacterial signalling molecule lumichrome enhances plant growth through a combination of enhanced cell division and cell enlargement, and possibly enhances photosynthesis.
Lumichrome (7,8 dimethylalloxazine), a novel multitrophic signal molecule produced by Sinorhizobium meliloti bacteria, has previously been shown to elicit growth promotion in different plant species (Phillips et al. in Proc Natl Acad Sci USA 96:12275–12280, https://doi.org/10.1073/pnas.96.22.12275, 1999). However, the molecular mechanisms that underlie this plant growth promotion remain obscure. Global transcript profiling using RNA-seq suggests that lumichrome enhances growth by inducing genes impacting on turgor driven growth and mitotic cell cycle that ensures the integration of cell division and expansion of developing leaves. The abundance of XTH9 and XPA4 transcripts was attributed to improved mediation of cell-wall loosening to allow turgor-driven cell enlargement. Mitotic CYCD3.3, CYCA1.1, SP1L3, RSW7 and PDF1 transcripts were increased in lumichrome-treated Arabidopsis thaliana plants, suggesting enhanced growth was underpinned by increased cell differentiation and expansion with a consequential increase in biomass. Synergistic ethylene–auxin cross-talk was also observed through reciprocal over-expression of ACO1 and SAUR54, in which ethylene activates the auxin signalling pathway and regulates Arabidopsis growth by both stimulating auxin biosynthesis and modulating the auxin transport machinery to the leaves. Decreased transcription of jasmonate biosynthesis and responsive-related transcripts (LOX2; LOX3; LOX6; JAL34; JR1) might contribute towards suppression of the negative effects of methyl jasmonate (MeJa) such as chlorophyll loss and decreases in RuBisCO and photosynthesis. This work contributes towards a deeper understanding of how lumichrome enhances plant growth and development.
KeywordsCell wall Cyclins Defence response Expansins Mitotic cell cycle Stress response Transcript profiling
Plant growth-promoting rhizobacteria
We are very grateful to Professor Martin Kidd for aid in the statistical analysis. Computations were performed using the University of Stellenbosch Central Analytical Facilities’ HPC2: http://www.sun.ac.za/hpc.
This research was funded by the National Research Foundation (SARChi Research Chair “Genetic tailoring of biopolymers”) of South Africa.
Compliance with ethical standards
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
- Abel S, Nguyen MD, Chow W, Theologis A (1995) ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J Biol Chem 270:19093–19099CrossRefPubMedGoogle Scholar
- Chauvin A, Caldelari D, Wolfender JL, Farmer EE (2013) Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for LIPOXYGENASE 6 in responses to long-distance wound signals. New Phytol 197:566–575. https://doi.org/10.1111/nph.12029 CrossRefPubMedGoogle Scholar
- Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533 CrossRefGoogle Scholar
- Kuluev BR, Knyazev AB, Lebedev YP, Chemeris AV (2012) Morphological and physiological characteristics of transgenic tobacco plants expressing expansin genes: AtEXP10 from Arabidopsis and PnEXPA1 from poplar. Russ J Plant Physiol 59:97–104. https://doi.org/10.1134/S1021443712010128 CrossRefGoogle Scholar
- Lu P, Porat R, Nadeau JA, O’Neill SD (1996) Identification of a meristem L1 layer-specific gene in Arabidopsis that is expressed during embryonic pattern formation and defines a new class of homeobox genes. Plant Cell 8:2155–2168. https://doi.org/10.1105/tpc.8.12.2155 CrossRefPubMedPubMedCentralGoogle Scholar
- Matiru VN, Dakora FD (2005a) Xylem transport and shoot accumulation of lumichrome, a newly recognized rhizobial signal, alters root respiration, stomatal conductance, leaf transpiration and photosynthetic rates in legumes and cereals. New Phytol 165:847–855. https://doi.org/10.1111/j.1469-8137.2004.01254.x CrossRefPubMedGoogle Scholar
- Muñoz-Bertomeu J, Cascales-Miñana B, Mulet JM et al (2009) Plastidial glyceraldehyde-3-phosphate dehydrogenase deficiency leads to altered root development and affects the sugar and amino acid balance in Arabidopsis. Plant Physiol 151:541–558. https://doi.org/10.1104/pp.109.143701 CrossRefPubMedPubMedCentralGoogle Scholar
- Thomma BPHJ, Eggermont K, Penninckx IAMA et al (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111. https://doi.org/10.1073/pnas.95.25.15107 CrossRefPubMedGoogle Scholar
- Wolf S, Hématy K, Höfte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407. https://doi.org/10.1146/annurev-arplant-042811-105449 CrossRefPubMedGoogle Scholar