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Involvement of the 4-coumarate:coenzyme A ligase 4CL4 in rice phosphorus acquisition and rhizosphere microbe recruitment via root growth enlargement

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Abstract

Main conclusion

The 4-coumarate:coenzyme A ligase 4CL4 is involved in enhancing rice P acquisition and use in acid soil by enlarging root growth and boosting functional rhizosphere microbe recruitment.

Abstract

Rice (Oryza sativa L.) cannot easily acquire phosphorus (P) from acid soil, where root growth is inhibited and soil P is fixed. The combination of roots and rhizosphere microbiota is critical for plant P acquisition and soil P mobilization, but the associated molecular mechanism in rice is unclear. 4CL4/RAL1 encodes a 4-coumarate:coenzyme A ligase related to lignin biosynthesis in rice, and its dysfunction results in a small rice root system. In this study, soil culture and hydroponic experiments were conducted to examine the role of RAL1 in regulating rice P acquisition, fertilizer P use, and rhizosphere microbes in acid soil. Disruption of RAL1 markedly decreased root growth. Mutant rice plants exhibited decreased shoot growth, shoot P accumulation, and fertilizer P use efficiency when grown in soil—but not under hydroponic conditions, where all P is soluble and available for plants. Mutant ral1 and wild-type rice rhizospheres had distinct bacterial and fungal community structures, and wild-type rice recruited some genotype-specific microbial taxa associated with P solubilization. Our results highlight the function of 4CL4/RAL1 in enhancing rice P acquisition and use in acid soil, namely by enlarging root growth and boosting functional rhizosphere microbe recruitment. These findings can inform breeding strategies to improve P use efficiency through host genetic manipulation of root growth and rhizosphere microbiota.

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Data availability

The raw data for rhizosphere microbiota were submitted to the NCBI BioProject database under accession number PRJNA821392. Further detailed data that support the findings of this study are available from the corresponding author upon reasonable request.

Abbreviations

4CL:

4-Coumarate:coenzyme A ligase

RAL1:

Resistance to aluminum 1

OTU:

Operational taxonomic unit

NMDS:

Non-metric multi-dimensional scaling

ANOSIM:

Analysis of similarities

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Acknowledgements

We are grateful to C-F Huang for providing rice seed materials and nice comments on this study. We thank HZ, JL, XL, and YW: for their assistance with rice cultivation and soil sampling. We thank LB (Edanz) (www.liwenbianji.cn/ac) for editing the English text of a draft of this manuscript.

Funding

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (nos XDA24020104 and XDA24040203) and the National Natural Science Foundation of China (nos. 42077101 and 31672229).

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Authors and Affiliations

  1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Xun Xiao, Xiao Ying Dong, Ren Fang Shen & Xue Qiang Zhao

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xun Xiao, Ren Fang Shen & Xue Qiang Zhao

  3. School of Geographical Science, Nantong University, Nantong, 226019, China

    An Yong Hu

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425_2023_4158_MOESM1_ESM.docx

Supplementary file 1: Table S1 Primers used for detection of Pi starvation response gene expression. Table S2 Primers and thermal cycling protocols used for high-throughput sequencing. Table S3 Analysis of similarities (ANOSIM) test of the effects of P level and genotype on the beta diversity of bacterial and fungal community structures based on Bray–Curtis distance matrixes. Table S4 Mantel test of the correlation between selected soil and rice properties based on Euclidean distances and rhizosphere microbiological structure based on Bray–Curtis distances. Table S5 Bacterial and fungal OTUs enriched in the rhizosphere of Kasalath and ral1 under non-liming (-Ca) and liming (+ Ca) conditions. Table S6 Key topological features of co-occurrence network patterns under non-liming (-Ca) and liming (+ Ca) conditions. Table S7 Relative abundance and taxonomy of hub species in co-occurrence networks. Fig. S1 The general biosynthesis pathway of lignin in higher plants modified from Liu et al. (2018). Green words indicate the specific step of 4CL4 involved in lignin biosynthesis. PAL, phenylalanine ammonia-lyase; TAL, tyrosine ammonia-lyase; C4H, cinnamate 4-hydroxylase; 4CL, 4-coumarate: CoA ligase; CCR, cinnamoyl-CoA reductase; HCT, hydroxycinnamoyl-CoA shikimate/Quinatehydroxycinnamoyltransferase; C3H, p-coumarate 3-hydroxylase; CCoAOMT, caffeoyl-CoA O-methyltransferase; F5H, ferulate 5-hydroxylase; CSE, caffeoyl shikimate esterase; COMT, caffeic acid O-methyltransferase; CAD, cinnamyl alcohol dehydrogenase; LAC, laccase; POD, peroxidase. Fig. S2 Shoot growth picture of Kasalath and ral1 under the soil culture experiment. 10-day-old seedlings were grown in soil supplemented with 0, 10, or 50 mg kg−1 P under liming (+ Ca) or non-liming (-Ca) conditions for 40 days. Fig. S3 Short-term P uptake rate of wild-type Kasalath rice and its mutant ral1. Sixteen-day-old seedlings were exposed to 10 or 180 μM P for 4 h. Asterisks indicate significant differences between Kasalath and ral1 at the same P level (P < 0.05, independent-sample t-test). Data are means ± standard deviation (n = 4). Fig. S4 Gene expression related to rice P starvation responses. 10-day-old rice plants were exposed to half-strength Kimura B solution (pH 4.6) containing 5, 20, 90, or 180 μM P for 10 days, and then roots were sampled for the expression analysis. Expression level relative to Kasalath with 90 μM P is shown. Different uppercase and lowercase letters above bars indicate significant differences among different P levels for Kasalath and ral1, respectively (P < 0.05, Duncan’s multiple range test). Asterisks indicate significant differences between Kasalath and ral1 under the same treatment conditions (P < 0.05, independent-sample t-test). Data are means ± standard deviation (n = 3). Fig. S5 Richness and Shannon diversity indexes of bacteria (a, c) and fungi (b, d) in rhizosphere soils of wild-type Kasalath rice and its mutant ral1 at different P levels under liming (+ Ca) and non-liming (-Ca) conditions. Different uppercase and lowercase letters above bars indicate significant differences among different P levels for Kasalath and ral1, respectively (P < 0.05, Duncan’s multiple range test). Data are means (n = 4). Fig. S6 Non-metric multi-dimensional scaling (NMDS) analysis of bacterial (a) and fungal (b) community structure based on a Bray–Curtis dissimilarity matrix. Fig. S7 Stamp analysis of the relative abundance of bacterial (a, b) and fungal (c, d) phyla at the 95% confidence interval level between Kasalath and ral1 under liming (+ Ca) and non-liming (-Ca) conditions. Fig. S8 Soil chemical properties of rhizospheres of Kasalath and ral1 at different P levels under liming (+ Ca) and non-liming (-Ca) conditions. a Soil pH. b Bray P. c Exchangeable Al. Different uppercase and lowercase letters above bars indicate significant differences among different P levels for Kasalath and ral1, respectively (P < 0.05, Duncan’s multiple range test). Asterisks indicate significant differences between Kasalath and ral1 under the same treatment conditions (P < 0.05, independent-sample t-test). Data are means ± standard deviation (n = 4) (DOCX 8032 KB)

425_2023_4158_MOESM2_ESM.xlsx

Supplementary file 2: Table S5 Bacterial and fungal OTUs enriched in the rhizosphere of Kasalath and ral1 under non-liming (-Ca) and liming (+ Ca) conditions (XLSX 55 KB)

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Xiao, X., Hu, A.Y., Dong, X.Y. et al. Involvement of the 4-coumarate:coenzyme A ligase 4CL4 in rice phosphorus acquisition and rhizosphere microbe recruitment via root growth enlargement. Planta 258, 7 (2023). https://doi.org/10.1007/s00425-023-04158-4

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