- Open Access
Rhizosphere microorganisms can influence the timing of plant flowering
- Tao Lu†1,
- Mingjing Ke†1,
- Michel Lavoie2,
- Yujian Jin1,
- Xiaoji Fan1,
- Zhenyan Zhang1,
- Zhengwei Fu3,
- Liwei Sun1,
- Michael Gillings4,
- Josep Peñuelas5, 6,
- Haifeng Qian1, 7Email authorView ORCID ID profile and
- Yong-Guan Zhu8, 9Email author
© The Author(s). 2018
- Received: 15 September 2018
- Accepted: 17 December 2018
- Published: 26 December 2018
Plant phenology has crucial biological, physical, and chemical effects on the biosphere. Phenological drivers have largely been studied, but the role of plant microbiota, particularly rhizosphere microbiota, has not been considered.
We discovered that rhizosphere microbial communities could modulate the timing of flowering of Arabidopsis thaliana. Rhizosphere microorganisms that increased and prolonged N bioavailability by nitrification delayed flowering by converting tryptophan to the phytohormone indole acetic acid (IAA), thus downregulating genes that trigger flowering, and stimulating further plant growth. The addition of IAA to hydroponic cultures confirmed this metabolic network.
We document a novel metabolic network in which soil microbiota influenced plant flowering time, thus shedding light on the key role of soil microbiota on plant functioning. This opens up multiple opportunities for application, from helping to mitigate some of the effects of climate change and environmental stress on plants (e.g. abnormal temperature variation, drought, salinity) to manipulating plant characteristics using microbial inocula to increase crop potential.
- Root exudate
- Indole acetic acid
- Flowering time
Climate change has altered plant phenology [1, 2]. This has crucial biological, physical, and chemical effects on the biosphere and the earth system . These phenological alterations have become a subject of great interest in ecological and environmental sciences. Changes to phenology have been attributed to multiple factors, including warming , but the role of plant microbiota and particularly rhizosphere microbiota has not been considered. And yet, the rhizosphere harbors a diverse community of microorganisms that play critical roles in plant growth and reproduction [5, 6].
We know that rhizosphere microbiota protect against pathogens, improve growth by producing phytohormones, and may help plants withstand environmental perturbations such as abnormal variation in temperature, drought, and salinity related to climate [7–10]. Recent studies also suggest that root microbiota can contribute to phenotypic plasticity, which has important implications for our understanding of plant phenology in a changing climate and for increasing crop production [11, 12]. Several auxins have decisive functions in the establishment of plant developmental and reproductive programs [13, 14]. Auxins can be synthesized by rhizosphere microorganisms [15, 16], raising the intriguing possibility that root microbiota may regulate plant growth and development through phytohormone production.
Understanding the interactions between plant microbiota, root exudation, and plant growth and reproduction, however, remains limited, despite significant advances in the last decade . Root exudates account for 5–21% of total photosynthetically fixed carbon and help drive the composition of rhizosphere communities [18, 19]. Exudates may be excess plant products [20, 21], but they can also contain signaling and chemoattractant molecules. These molecules recruit beneficial microorganisms that contribute to pathogen resistance, water retention, and the synthesis of growth-promoting hormones , and may influence plant phenotype .
Interactions between exudates, soil microbiota, and plant physiology have the potential to dynamically affect rhizospheric communities and alter plant phenotypes by complex feedback mechanisms. We studied the molecular interactions among root exudates, rhizosphere microbiota, and plant physiology in wild-type (Wt) and mutant (pgr5) plants of Arabidopsis thaliana (hereafter Arabidopsis) and identified a novel network of molecular interactions linking the nitrogen cycle, the phytohormone IAA produced from Tryptophan (Trp), and the timing of flowering. These results thus provide evidence of an outstanding phenomenon: the timing of plant flowering may be influenced by soil microbiota.
Rhizosphere microbiota can delay the onset of flowering of Wt Arabidopsis
The richness and diversity of the rhizosphere microorganisms tended to decrease in parallel with the changes in Arabidopsis physiology over the three generations. Species richness and diversity based on four indices (Chao1, abundance-based coverage (ACE), number of species, and the Shannon index) significantly decreased after the two and three generations (Fig. 1b and Additional file 1: Figure S1). The relative abundances of Proteobacteria and Acidobacteria, the dominant bacterial phyla in the rhizosphere, decreased by generations 2 and 3 relative to generation 1. In contrast, Bacteroidetes and cyanobacterial abundances increased by generation 3 (Fig. 1c and Additional file 2). It was demonstrated that some early (or late)-flowering plant could be associated to specific soil microorganism families  and that plant microbiota could be associated with changes in different plant growth phases . The results suggest that the selected enriched microbes during the three generations play crucial roles in modulating plant flowering time.
Rhizosphere microbiota advanced the flowering time of the pgr5 mutant
To better understand the relationships between microbiota, exudates, and flowering time, we used an Arabidopsis mutant (for the PGR5 gene that encodes a novel thylakoid membrane protein) that grows as well as Wt plants in the vegetative phase [28, 29]. The pgr5 mutant is deficient in antimycin A-sensitive cyclic flow from ferredoxin to plastoquinone, which is one of the most crucial physiological processes for efficient photosynthesis . Because of defects in photosynthesis, the pgr5 mutant produces different exudates from the Wt Arabidopsis. The phenotype of the pgr5 mutant was unchanged in generations 1 and 2 in the group treated with pgr5 microbiota (pgr5-M) compared to the corresponding control (without the addition of soil microbiomes), as for the Wt Arabidopsis. The flowering time of the pgr5-M-treated group, however, was nearly 4 days earlier by generation 3, in contrast to Wt, and the silique number was significantly lower (Additional file 1: Table S1). The changes in plant reproduction induced by the microbial manipulations were probably not driven by rhizosphere diversity, because the Shannon and richness indices of the pgr5-M- and Wt-M-treated groups did not generally differ over the three generations (Additional file 1: Figure S1). The ACE data, though, differed after one generation (Fig. 1b). The relative abundances of the phyla differed only marginally between the two Arabidopsis lines in each generation (Fig. 1c).
Rare rhizosphere microbes potentially affected flowering time
The abundances of microbial phyla were relatively constant (see above), but abundances between the WM- (microbiota from the third-generation Wt cultures) and the PM (microbiota from the third-generation pgr5 cultures)-treated groups differed more at lower taxonomic levels. The relative abundances of 77 rhizosphere genera differed significantly between the WM and PM treatment by generation 3, by at least a factor of two. A total of 41 genera were enriched in the WM treatment relative to the PM treatment, and 36 genera were enriched in the PM treatment (Additional file 1: Table S2 and Additional file 3).
Most of the enriched rhizosphere microorganisms were initially rare (relative abundance < 1%), such as Emticicia, Methylobacterium, and Filimonas, suggesting that rare rhizosphere microbes might play a role in modulating Arabidopsis flowering. Rare microbes can be involved in soil biochemical processes and as active modulators of plant growth and resistance to pathogens . The enriched microbes in the WM treatment mostly have key roles in rhizosphere N regeneration or in maintaining plant growth (Additional file 1: Table S3) [16, 31–34]. Indeed, Bacillus, enriched in the WM treatment, can potentially contribute to soil N fixation . Potential denitrifying organisms such as Stenotrophomonas and Emticicia, though, were enriched in the PM treatment [31, 36]. We hypothesize that an increase in N fixation and cycling in Wt Arabidopsis associated with the microbiota, and the potential increase in denitrification in the pgr5 mutant, could help increase the duration of N bioavailability in Wt Arabidopsis relative to the pgr5 mutant. Plant pathogenic genera enriched in PM, such as Panacagrimonas and Filimonas, may also contribute to the earlier flowering time, because infected hosts preferentially allocate resources toward reproduction [37, 38]. This hypothesis linking N availability to flowering time is discussed further below within the newly proposed molecular network that modulates flowering time.
Verification of microbial function
The addition of the two soil slurries did not change bulk-soil pH, available soil K or P contents (Additional file 1: Table S4), the abundance of key genes involved in the C cycle, or the activities of β-glucosidase or chitinase in the rhizosphere (Additional file 1: Figure S2 and S3) but did affect the abundance of genes (normalized to the abundance of 16S rRNA gene) involved in N cycling (Fig. 2e–h) and the amounts of NH4+ (Fig. 3A) and NO3− (Fig. 3C) in soil. The concentration of bioavailable N species was generally lower after the addition of the pgr5 microbiota compared to the treatment with the addition of Wt microbiota (Fig. 3A, C). This decrease in N availability in the cultures treated with pgr5 microbiota was accompanied by an increase in the abundance of genes involved in denitrification (nirK and nosZ) and a decrease in the abundance of genes involved in nitrogen fixation (nifH) and nitrification (amoA) compared to the Wt-treated groups (Fig. 2e–h). In the Wt-treated group, the activity of urease was higher (Fig. 3B) and nitrate reductase was lower (Fig. 3D) than those in the PM group, which probably resulted in higher NH4+ and NO3−.
Several lines of evidence support the hypothesis that the rhizosphere microbiota modulated N cycling and bioavailability, leading to N deficiency earlier in the pgr5-treated groups and thus earlier flowering. Flowering can be triggered by low nitrate levels , but plants maximize growth before flowering under the conditions of N sufficiency .
Different root exudates in the two Arabidopsis lines
Trp and its derivatives, phenols, and some carboxylic acids were preferentially exuded in the Wt cultures (Additional file 1: Table S5). The concentrations of amino acids were generally higher in the Wt cultures, consistent with a higher abundance of Bacillus subtilis in the Wt cultures, for which amino acids are chemoattractants. These metabolomic results are consistent with the hypothesis that differences in exudates affect rhizosphere microbiota .
IAA delayed flowering time by downregulating genes involved in flowering
Auxins regulate plant growth in many ways [13, 41, 42]. One of the important auxins for plants is IAA, which is soluble in aqueous solutions and, when protonated, diffuses passively across cell membranes without the need of a specific transporter . IAA has also been hypothesized to have a floral-inductive signaling role by regulating multiple aspects of embryonic and postembryonic development [44, 45]. Microorganisms can produce IAA from Trp [46–49]. One of the enriched rhizosphere microorganisms, Arthrobacter (Additional file 1: Table S3), has been reported to be beneficial for plant growth by having the ability to produce IAA . Trp and its derivatives were enriched in the Wt exudates, so the generation of IAA by microorganisms may control flowering time by a novel molecular network. Trp content in the soil of generation 3 of the Wt cultures decreased, and the IAA content increased 3.03-fold, suggesting that the Wt microbiota rapidly converted Trp into IAA (Fig. 4c, d).
Shimada et al.  reported that IAA relieved the inhibitory effects of aspterric acid on pollen growth and thus speculated that IAA accelerated reproductive growth in Arabidopsis. To our knowledge, our microcosm study is the first to demonstrate that IAA is one critical signal that delays flowering in Arabidopsis, although Wagner et al.  also found a similar phenomenon, while not proposing any related mechanism.
Combined with earlier reports, the weight of evidence suggests that IAA stimulates the development of floral organs but delays the flowering time of Arabidopsis. Our data strongly suggest that IAA delays flowering and acts as a signal of optimal growth conditions in the absence of N limitation for growth.
Arabidopsis seeds (wild-type Col-0 (Wt) and the pgr5 mutant, deficient in PGR5-dependent cyclic electron flow from ferredoxin to plastoquinone), were surface sterilized to avoid bacterial contamination on solid medium and vernalized as described by Sun et al. . Given that photosynthesis is the main resource of exudates, photosystem mutant with the same genetic background with that of Wt was selected to induce different exudates. Vernalized seeds were cultured in Petri dishes containing Murashige and Skoog (MS) medium under sterile conditions at 25 °C at a light intensity of 300 μmol photons/m2/s and a 12:12-h light to dark photoperiod. The MS medium containing 3% sugar and 0.5% agar was autoclaved at 115 °C for 30 min before use. Two-week-old aseptic seedlings were transplanted into polycarbonate pots (400 mL) containing autoclaved potting-mix soil (Sun Gro Horticulture, MA, USA).
Microcosm experiments across generations
Approximately 30 g of grassland soil collected near the Zhejiang University of Technology, China (30° 17′ 45.11″ N, 120° 09′ 50.07″ E) was mixed with 200 mL of sterile water by vigorous shaking for 60 s . Ten-milliliter samples of soil slurry were added to polycarbonate pots transplanted with 20 seedlings of either the Wt or the pgr5 Arabidopsis line. Nine replicate pots were used for generation 1 for each line and for a control treatment (n = 9) without added soil slurry. Plants grew in an artificial greenhouse at 25 ± 0.5 °C and 80% relative humidity under cool-white fluorescent light (300 μmol photons/m2/s) with a 12:12-h light to dark cycle.
The plants and soils were harvested when 80% of the plants had floral buds of 1 ± 0.1 cm or larger (measured from the center of the rosette), and the time to flowering was recorded. Large soil aggregates that were loosely bound to the roots were first removed by shaking, and 30 g of the tightly bound rhizosphere soil was then collected (see the “Collection of rhizosphere soil” section) and added to 200 mL of sterile water, producing a soil slurry for generation 1. This slurry was used for inoculating the Arabidopsis lines for the second and third generations, as described above. Treatments inoculated with the microbiota of Wt and the pgr5 mutant were designated WM and PM, respectively. The generations in our study refer to the propagation of soil microbes only, and all seeds were from a common stock. At flowering stage and harvest time, the physiological parameters including the number of days before flowering, fresh weight, number of rosette leaves, and number of siliques were determined in wild-type (Wt) and pgr5 mutant ecotypes grown in microcosms for each generation.
Collection of rhizosphere soil
Rhizosphere soil was collected as described by Bulgarelli et al. . Four-centimeter sections of roots were collected immediately below the rosette, and the roots from each pot were transferred to a 50-mL centrifuge tube containing 20 mL of sterile phosphate buffer saline (PBS; 137 mM sodium chloride, 10 mM phosphate buffer, 2.7 mM potassium chloride; pH 7.3–7.5). The centrifuge tubes were shaken at 40 g for 20 min on an orbital shaker. The roots were removed, the solution was centrifuged at 1000g for 20 min, and the pellet of rhizosphere soil was recovered. All samples of rhizosphere soil were frozen in liquid nitrogen and stored at − 80 °C until analysis.
16S rRNA gene sequencing
The frozen soil samples were thawed on ice, and DNA was extracted using a PowerSoil DNA Isolation Kit (MO BIO Laboratories, Inc., Carlsbad, USA). 16S rRNA genes were amplified using EXtaq enzyme (TaKaRa, Kyoto, Japan) and the specific primers 314F (5′-CCTACGGGNGGCWGCAG-3′) and 805R (5′-GACTACHVGGGTATCTAATCC-3′) with the adapter (index) that targets the V3 and V4 variable regions of bacterial/archaeal 16S rRNA genes. Strongly amplified products 460 bp in length were chosen for further experiments. The amplicons were quantified with a Qubit 2.0 fluorometer (Thermo Fisher Scientific, USA), diluted to 1 ng/μL, and sequenced on a MiSeq platform (PE250). In total, 854,514 raw reads were obtained from the 18 samples of rhizosphere soils (6 groups as shown in Fig. 1a, n = 3). We computed operational taxonomic units (OTU) and microbial diversity as described previously . Rarefaction curves of observed species are shown in Additional file 1: Fig. S5.
Analysis of rhizosphere DNA abundance by quantitative real-time PCR (qRT-PCR)
Rhizosphere DNA was quantified by ultraviolet-visible spectrophotometry (ND 5000, BioTeke, China) and diluted to 10 ng/μL. The abundances of rhizosphere genes (amoA, nifH, nirK, nosZ, cbbL, β-glu, and ChiA; Additional file 1: Table S6) were measured in 10-μL PCRs containing 5 μL of SYBR Green Real-time PCR Master Mix (Toyobo, Tokyo, Japan), 0.4 μL of each of the forward and reverse primers (10 mM) (see Additional file 1: Table S6 for a list of primers), 1 μL of rhizosphere DNA at 10 ng/L, and 3.2 μL of ddH2O. The qRT-PCR protocol was 94 °C for 3 min followed by 40 cycles of 94 °C for 30 s, 56 °C for 30 s, and 72 °C for 1 min on an Eppendorf MasterCycler ep RealPlex (Wesseling-Berzdorf, Germany).
Measurements in the dissolved phase of the soil samples
Physicochemical (nutrient contents and pH) and biological (enzymatic activities and concentrations of IAA and Trp) variables were measured in the dissolved phase of the soil samples. After three generations of Arabidopsis cultures (Fig. 1a), soil samples were then collected randomly from each pot, air-dried, homogenized, and sieved to obtain particles < 1 mm. The activity of soil enzymes (β-glucosidase, chitinase, urease, and nitrate reductase) and soil N content (NH4+ and NO3− contents) were subsequently measured using 0.5 g of soil (n = 4) following the manufacturer’s instructions of corresponding commercial reagent kits (COMIN, Suzhou, China). The concentrations of two key metabolites (IAA and Trp) were measured in the soil dissolved phase. Five grams of soil was mixed with 5 g of NaCl and 20 mL of acetonitrile for 5 min, followed by centrifugation at 1000g for 10 min. The concentrations of IAA and Trp in the supernatants were measured by Liquid Chromatography-Electrospray Ionization-Mass/Mass Spectroscopy (LC-ESI-MS/MS, Q-Trap 5500, Agilent Technologies, USA).
Collection, measurement, and identification of root exudates
Arabidopsis seedlings (Wt and pgr5 mutant) reached the bolting stage after approximately 40 days of culture and were then transferred to glass containers containing 40 mL of ddH2O . After 3 days of culture in the glass containers, culture media containing exudates were passed through 0.45-μm filter membranes. Approximately 35 mL of the solution was freeze-dried, dissolved in 500 μL of 80% methanol, and derivatized with Bis (trimethylsilyl) trifluoroacetamide and 1% chlorotrimethylsilane. The derivatized samples were analyzed by gas chromatography/mass spectroscopy GC-MS (Agilent 7890B gas chromatographic system coupled to an Agilent 5977A Mass Spectrometry Detector (Agilent, USA)). The potential involvement of all identified exudates in Arabidopsis biochemical pathways was subsequently determined by reference to the KEGG database .
Addition of Trp, 5-hydroxytryptophan (5-HTP), and IAA and analysis of gene transcription associated with flowering
For hydroponic experiments (i.e., plants cultured in solution), Trp, 5-HTP, and IAA were added to autoclaved liquid MS medium cultured with Wt at final concentrations of 0.5, 5, and 25 nM, respectively. Control cultures without Trp, 5-HTP, and IAA were performed in parallel. The transcription of genes involved in flowering was measured by qRT-PCR. Control groups treated with Trp, 5-HTP, and IAA were analyzed at three stages of development: (1) early flowering (when 10% of control plants had floral buds), (2) intermediate flowering (when > 50% of control plants had floral buds), and (3) late flowering (when > 80% of control plants had floral buds) stages. Total RNA was isolated from the plants and then reverse transcribed into cDNA for qRT-PCR analysis using the protocol described by Chen et al.  and the primer pairs in Additional file 1: Table S6. We studied the transcription of six genes in the autonomous pathway (FCA, FLD, FPA, FVE, FY, and LD), three genes in the gibberellin acid (GA) pathway (GAI, GA1, and RGA), six genes in the vernalization pathway (FR1, VRN1, VRN2, VIN3, and PIE1), five genes in the photoperiod pathway (CCA1, CO, GI, LHY, and TOC1), and five genes in the floral integrator pathway (FLC, FT, SOC1, AGL-24, LFY, and AP1).
Data analysis and statistical methods
For the biochemical and physiological measurements, analysis of variance followed by the Dunnett’s post hoc test was performed to evaluate the statistical significance among data using the StatView 5.0 program (Statistical Analysis Systems Institute, Cary, NC, USA). Means among treatments were considered significantly different, when the probability (p) was less than 0.05. All analyses were performed in triplicate unless otherwise stated. All data are presented in the tables and figures as mean ± SD (standard deviation).
We sincerely thank all the authors who provided valuable data or comments for this study. We are very thankful to Dr. Tsuyoshi Endo and Professor Fumihiko Sato (Kyoto University, Japan) who provided the pnsB4 and pgr5 mutant lines of Arabidopsis thaliana.
This work was financially supported by the National Natural Science Foundation of China (21577128, 21777144), the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB15020302 and XDB15020402), the CAS Pioneer Hundred Talents Program (H.F. Qian), and the Xingjiang Uighur Autonomous Region Talent Project (H.F. Qian). JP research is funded by the European Research Council Synergy grant SyG-2013-610028 IMBALANCE-P.
Availability of data and materials
All data needed to evaluate the conclusions in the paper are present in the paper and/or the supplementary materials. The raw data of 16S rRNA gene sequences have been submitted to the NCBI Sequence Read Archive (SRA) database under the BioProject number PRJNA494813.
HFQ, ZWF, and YGZ designed the study; TL, MJK, YJJ, XJF, and ZYZ performed the research; HFQ, TL, MJK, YJJ, LWS, and YGZ analyzed the data; and HFQ, TL, YJJ, ML, MG, JP, and YGZ wrote the manuscript. All authors read and approved the final manuscript.
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