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Chloroplast elongation factors break the growth–immunity trade-off by simultaneously promoting yield and defence

Nature Plants volume 10, pages 1576–1591 (2024)Cite this article

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Abstract

Chloroplasts regulate plant development and immunity. Here we report that potato chloroplast elongation factors StTuA and StTuB, targeted by Phytophthora infestans RXLR effector Pi22926, positively regulate immunity and growth. Plants expressing Pi22926, or silenced for TuA/B, show increased P. infestans susceptibility and decreased photosynthesis, plant growth and tuber yield. By contrast, StTuA/B overexpression reduces susceptibility, elevates chloroplast-derived reactive oxygen species production and increases photosynthesis and potato tuber yield by enhancing chloroplast protein translation. Another plant target of Pi22926, StMAP3Kβ2, interacts with StTuB, phosphorylating it to promote its translocation into chloroplasts. However, Pi22926 attenuates StTuB association with StMAP3Kβ2 and phosphorylation. This reduces StTuB translocation into chloroplasts, leading to its proteasome-mediated turnover in the cytoplasm. We uncover new mechanisms by which a pathogen effector inhibits immunity by disrupting key chloroplast functions. This work shows that StTuA/B break the growth–immunity trade-off, promoting both disease resistance and yield, revealing the enormous potential of chloroplast biology in crop breeding.

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Fig. 1: Stable expression of effector Pi22926 in potato inhibits plant growth and reduces late blight resistance.
Fig. 2: Pi22926 interacts with StTuA and StTuB in the host cytoplasm.
Fig. 3: StTuA and StTuB function as positive regulators of late blight resistance.
Fig. 4: StTuA and StTuB positively regulate immunity by the activation of ROS and PTI.
Fig. 5: Overexpression of StTuA and StTuB enhances photosynthesis, plant growth and tuber yield.
Fig. 6: Pi22926 promotes StTuA and StTuB degradation by the 26S proteasome.
Fig. 7: Pi22926 inhibits StTuB transfer into chloroplasts by inhibiting StMAP3Kβ2.
Fig. 8: A proposed model of Pi22926 inhibiting the function of StTuA/B and StMAP3Kβ2 during P. infestans infection to suppress immunity.

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Data availability

All data supporting the findings of this study are available in this published article (and its Supplementary Information files). The biological materials used in this study are available from Z.T. on reasonable request. Source data are provided with this paper.

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Acknowledgements

We acknowledge the financial support from the National Key R&D Program of China (grant no. 2023YFF1000404), the National Natural Science Foundation of China (grant nos. 32372172, 32072121, 31761143007 to Z.T.) and the Science and Technology Planning Projects of Zhejiang Province (grant no. 2024SSYS0100 to Y.Q.). P.R.J.B was supported by European Research Council (ERC) Advanced Grant PathEVome 787764; Biotechnology and Biological Sciences Research Council Grants BB/S003096/1, BB/P020569 and BB/L026880/1.

Author information

Authors and Affiliations

  1. National Key Laboratory for Germplasm Innovation and Utilization of Horticultural Crops, Huazhong Agricultural University (HZAU), Wuhan, China

    Yetong Qi, Jiahui Wu, Zhu Yang, Hongjun Li, Lang Liu, Xinyuan Sun, Xinya Wu, Jiahui Nie, Jing Zhou, Meng Xu, Xintong Wu, Ruimin Yu, Dong Cheng, Qingguo Sun, Huishan Qiu, Yingtao Zuo & Zhendong Tian

  2. Hubei Hongshan Laboratory (HZAU), Wuhan, China

    Yetong Qi & Zhendong Tian

  3. Key Laboratory of Potato Biology and Biotechnology (HZAU), Ministry of Agriculture and Rural Affairs, Wuhan, China

    Yetong Qi, Jiahui Wu, Zhu Yang, Hongjun Li, Lang Liu, Xinyuan Sun, Xinya Wu, Jiahui Nie, Jing Zhou, Meng Xu, Xintong Wu, Ruimin Yu, Dong Cheng, Qingguo Sun, Huishan Qiu, Yingtao Zuo & Zhendong Tian

  4. Potato Engineering and Technology Research Center of Hubei Province (HZAU), Wuhan, China

    Yetong Qi, Jiahui Wu, Zhu Yang, Hongjun Li, Lang Liu, Xinyuan Sun, Xinya Wu, Jiahui Nie, Jing Zhou, Meng Xu, Xintong Wu, Ruimin Yu, Dong Cheng, Qingguo Sun, Huishan Qiu, Yingtao Zuo & Zhendong Tian

  5. Xianghu Laboratory, Hangzhou, China

    Yetong Qi

  6. Northwest A&F University, Xianyang, China

    Haixia Wang

  7. Division of Plant Sciences, University of Dundee, At James Hutton Institute, Dundee, UK

    Susan Breen & Paul R. J. Birch

  8. Cell and Molecular Sciences, James Hutton Institute, Dundee, UK

    Petra C. Boevink & Paul R. J. Birch

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Contributions

Z.T., Y.Q. and P.R.J.B. planned and designed the research. Y.Q., J.W., Z.Y., H.L., L.L., H.W., X.S., Xinya Wu, J.N., J.Z., M.X., Xintong Wu, R.Y., D.C., Q.S., H.Q. and Y.Z. performed the experiments. Y.Q., S.B., P.R.J.B. and Z.T. wrote the paper with input from all authors. Y.Q., S.B., P.C.B., P.R.J.B. and Z.T. analysed data and revised the paper.

Corresponding author

Correspondence to Zhendong Tian.

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The authors declare no competing interests. On the basis of the results in this study, the authors have applied for patents (application no. 202210963447.3).

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Nature Plants thanks Dong-Lei Yang and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Phenotype of OE-Pi22926 transgenic N. benthamiana lines.

a, b, Western blots show the protein levels of GFP-Pi22926 in transgenic overexpression potato and N. benthamiana lines using anti-GFP antibody. Protein loading is indicated by Ponceau stain. The experiments were repeated at least twice with similar results. c, Representative OE-Pi22926 transgenic N. benthamiana and wild type N. benthamiana plants. Images taken at 4 w after planting. Scale bar, 2 cm. d, Graph showing that the heights of OE-Pi22926 lines were lower than that of N. b (n = 6 individual transgenic plants). e, Graph showing chlorophyll content of OE-Pi22926 transgenic N. benthamiana lines (n = 5 biological replicates). f, Graph showing biomass of OE-Pi22926 transgenic N. benthamiana lines (n = 6 individual transgenic plants). g, Representative images showing the P. infestans infection areas on OE-Pi22926 transgenic N. benthamiana leaves. Scale bar, 2 cm. h, Graph shows a significant increase in P. infestans lesion sizes in transgenic lines compared to N. benthamiana control which was measured at 4 dpi and 5 dpi (Three biological replicates, n = 40). Centre lines show the medians; box limits indicate the 25th and 75th percentiles; whiskers extend to 1.5 × the interquartile range from the 25th and 75th percentiles, each point represents the lesion area of an individual leaf with precise n numbers in figure. i Graph showing the flg22-induced ROS production in OE-Pi22926 N. benthamiana leaves (n = 8 biological replicates, error bars are ± SE). Leaves were treated with 10 μM flg22 before ROS production was measured. RLU, relative luminescence units. In d, e, f and g, data are presented as mean values +/− SEM with different asterisks refer to significant difference based on one-way ANOVA, comparing the mean of each column with the mean of the control N. b (* P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001). Exact P values are shown in source data with 95% confidence intervals.

Source data

Extended Data Fig. 2 TuA and TuB positively regulate plant immunity.

a, b, VIGS of both NbTuA and NbTuB in N. benthamiana significantly increased P. infestans lesion sizes compared to TRV2:GFP control (n represents the total number of measured lesions with 3 biological replicates, **** P < 0.0001, unpaired t test). Left leaves in (b) show the phenotype of VIGS plants. Right leaves are P. infestans infected leaf images under UV light. c–f, Graph shows a significant decrease in P. infestans lesion and sporangia after inoculation with HB0914-2 on StTuA-GFP and StTuB-GFP transgenic potato lines compared to the Desiree control (for sporangia counting, n = 9). g–j, Transgenic StTuA-GFP and StTuB-GFP N. benthamiana lines showed significantly increased late blight resistance. k, l, Transgenic N. benthamiana lines overexpressing StTuA-GFP and StTuB-GFP showed a significant decrease in P. capsici lesion size compared to the N. benthamiana (WT) control. In c-f, g, i, k, data are presented as mean values +/− SEM with different asterisks refer to significant difference based on one-way ANOVA, comparing the mean of each column with the mean of the control N. b (n represents the total number of measured lesions with 3 biological replicates, ** P < 0.01, *** P < 0.001, **** P < 0.0001). The white circle represents the P. capsici lesion area. h, j, l, representative leaf images taken under UV light. In a, c, e, g, I and k, centre lines show the medians; box limits indicate the 25th and 75th percentiles; whiskers extend to 1.5 × the interquartile range from the 25th and 75th percentiles, the top line represents maxima and bottom line represents minima, each point represents the lesion area of an individual leaf with precise n numbers in figures. Exact P values are shown in source data with 95% confidence intervals.

Source data

Extended Data Fig. 3 Formation of chloroplast stromules in StTuA/B overexpressing N. benthamiana leaves.

a, Chloroplast stromules (indicated by arrows) formed in leaves of OE-StTuB transgenic N. benthamiana lines. Transgenic N. benthamiana leaves were treated with 10 μM flg22, DMSO, H2O or P. infestans. Fluorescence was detected by confocal microscopy 30 min after flg22 treatment or 48 h after P. infestans infection. Bar = 5 μm. This experiment was repeated independently at least twice with similar results. b, Chloroplast stromules formed after flg22 treatment in N. benthamiana leaves transiently expressing StTuB-GFP or cTP-GFP. GFP fluorescence shows the expression of StTuB-GFP or cTP-GFP, and the merged images contain the fluorescence of GFP, RFP-H2B and chlorophyll. c, Graph shows the percentage of chloroplasts showing stromule formation in StTuB-GFP or cTP-GFP-expressing plants treated with flg22. Bar = 10 μm. Data are presented as mean values +/− SEM with different asterisks refer to significant difference based on unpaired t-test (*** P < 0.001, n = 5 biological replicates). Exact P values are shown in source data with 95% confidence intervals.

Source data

Extended Data Fig. 4 StTuA and StTuB overexpression increases potato plant height, chlorophyll content and N. benthamiana plant biomass.

a, Representative images of OE-StTuA, OE-StTuB and StTuA/B-RNAi transgenic and Desiree (WT) plants taken under white light, bar = 5 cm. b–d, Chlorophyll a/b content of OE-StTuA, OE-StTuB and StTuA/B-RNAi transgenic lines and control Desiree potato (n = 3 biological replicates). Data are presented as mean values +/− SEM with different asterisks refer to significant difference based on one-way ANOVA, comparing the mean of each column with the mean of the control Desiree (* P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001). Bar = 1 μm. e, Representative plants and leaves of OE-StTuB N. benthamiana transgenic lines and WT (left; N. b), bar = 5 cm. f, Bar graph shows a significant biomass increase in OE-StTuB transgenic lines compared to the WT control. Data are presented as mean values +/− SEM with different asterisks refer to significant difference based on one-way ANOVA, comparing the mean of each column with the mean of the control N. b (* P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001, n = 6 individual transgenic plants). Exact P values are shown in source data with 95% confidence intervals.

Source data

Extended Data Fig. 5 Overexpression of StTuA and StTuB enhances chloroplast protein translation.

a, Chloroplast protein synthesis efficiency in leaves of wild type (Desiree) and OE-StTuA/B transgenic potato plants. Total chloroplast protein was determined by antipuromycin (α-Pur) western blot following a 1- h time course after puromycin treatment. Western blot probed with anti-GFP shows the amount of StTuA/B-GFP in each sample. The protein loading in each lane was 90 μg. The experiment was repeated twice with similar results. b, Heatmap showing relative fold-changes of chloroplast protein from Desiree (WT) vs OE-StTuB (line 12, 18) plant leaves under light and flg22 treatment (from chloroplast proteomics data). The proteins in the red frame are related to photosynthesis, in the blue frame are enzymes linked to ROS production, and in the green frame are disease resistance-related proteins. c, The presence of PsbD, GLYK, FSD1, tAPX which appeared in the proteomics data (b) was confirmed by western blotting using chloroplast protein extraction from transgenic line OE-StTuB12 and 18). The amount of the protein loaded in each lane was 50 μg. Mean fold change of protein level of PsbD, GLYK, FSD1, tAPX from proteome mass spectrometry analysis was presented at the bottom of the band. All of protein level of WT under light and flg22 was normalised to 1.00. The experiments were repeated independently at least twice with similar results.

Source data

Supplementary information

Supplementary Information

Supplementary Figs. 1–17 with figure legends and unprocessed blots in Supplementary Figs. 1, 2, 9, 11, 13–16.

Reporting Summary

Supplementary Tables

Supplementary Table 1. Targets of Pi22926 by Y2H screening. Supplementary Table 2. PSMs of TuA with and without cTP. Supplementary Table 3. The sequence of StTuA/B-RNAi, StTuA-RNAi and StTuB-RNAi fragment. Supplementary Table 4. Proteome sequencing data of StTuB12/18 under light and flg22 treatment. Supplementary Table 5. Primers used to construct vectors and RT–qPCR. Supplementary Table 6. Information on genes used in the paper.

Supplementary Data

Statistical source data for Supplementary Figs. 4–6, 8, 10, 12 and 15.

Source data

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Source Data Extended Data Fig. 1

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Qi, Y., Wu, J., Yang, Z. et al. Chloroplast elongation factors break the growth–immunity trade-off by simultaneously promoting yield and defence. Nat. Plants 10, 1576–1591 (2024). https://doi.org/10.1038/s41477-024-01793-x

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