INTERORGANELLE COMMUNICATION IN PLANT STRESS ADAPTATION: MEMBRANE CONTACT SITES, RETROGRADE SIGNALING, AND METABOLIC REPROGRAMMING

  • Priya R. Nair Department of Pathology, Amrita Institute of Medical Sciences, Kochi, Kerala, India
  • Arjun S. Menon Department of Biotechnology, Manipal Academy of Higher Education, Manipal, Karnataka, India
  • Kavya P. Rao Department of Life Sciences, Savitribai Phule Pune University, Pune, Maharashtra, India
Keywords: Interorganelle communication, membrane contact sites, retrograde signaling, metabolic reprogramming, abiotic stress, plant stress resilience

Abstract

Environmental stress requires plants to communicate between chloroplasts, mitochondria, the endoplasmic reticulum, peroxisomes, vacuoles, and the nucleus in a well-coordinated manner to keep cells in homeostasis. In this review, the role of interorganelle communication, involving membrane contact sites, retrograde signaling and metabolic reprogramming processes, in plant stress adaptation is discussed. Membrane contact sites convey the exchange of lipids, ions, metabolites and signaling molecules, and retrograde pathways convey the status of organelle function to the nucleus and redirect gene expression. These processes are mediated by major molecular messengers, such as reactive oxygen species, redox signals, calcium, lipids, metabolites and phytohormones. Interorganelle crosstalk also drives coordinated adjustments in photosynthesis, respiration, photorespiration, carbon and nitrogen metabolism, membrane composition, antioxidant systems, and osmoprotective pathways. These responses are particularly important under drought, salinity, temperature extremes, high light, hypoxia, and combined stresses, where cellular energy and redox balance are frequently challenged. New technologies, such as live-cell imaging, genetically encoded biosensors, proximity labelling, organelle-resolved multi-omics and functional genomics, are advancing the spatial and temporal resolution of these networks. However, there are significant gaps in identification of plant-specific contact site components, signal specificity and field-level relevance. A systems-level understanding of organelle communication could help develop new approaches to engineering crops that are more metabolically flexible and resilient under increasingly variable environmental conditions without sacrificing growth, development, or productivity.

Downloads

Download data is not yet available.

References

1.Allan, C., Morris, R. J., & Meisrimler, C. N. (2022). Encoding, transmission, decoding, and specificity of calcium signals in plants. Journal of Experimental Botany, 73(11), 3372-3385.
2.Alves, H. L., Matiolli, C. C., Soares, R. C., Almadanim, M. C., Oliveira, M. M., & Abreu, I. A. (2021). Carbon/nitrogen metabolism and stress response networks–calcium-dependent protein kinases as the missing link? Journal of Experimental Botany, 72(12), 4190-4201.
3.Angon, P. B., Tahjib-Ul-Arif, M., Samin, S. I., Habiba, U., Hossain, M. A., & Brestic, M. (2022). How do plants respond to combined drought and salinity stress?—A systematic review. Plants, 11(21), 2884.
4.Aroca, A., García-Díaz, I., García-Calderón, M., Gotor, C., Márquez, A. J., & Betti, M. (2023). Photorespiration: regulation and new insights on the potential role of persulfidation. Journal of experimental botany, 74(19), 6023-6039.
5.Baillie, A. L., Falz, A. L., Müller-Schüssele, S. J., & Sparkes, I. (2020). It started with a kiss: monitoring organelle interactions and identifying membrane contact site components in plants. Frontiers in Plant Science, 11, 517.
6.Barreto, P., Koltun, A., Nonato, J., Yassitepe, J., Maia, I. D. G., & Arruda, P. (2022). Metabolism and signaling of plant mitochondria in adaptation to environmental stresses. International Journal of Molecular Sciences, 23(19), 11176.
7.Benavente, J. L., Siliqi, D., Infantes, L., Lagartera, L., Mills, A., Gago, F., ... & Albert, A. (2021). The structure and flexibility analysis of the Arabidopsis synaptotagmin 1 reveal the basis of its regulation at membrane contact sites. Life Science Alliance, 4(10), e202101152.
8.Bian, J., Su, X., Yuan, X., Zhang, Y., Lin, J., & Li, X. (2023). Endoplasmic reticulum membrane contact sites: cross-talk between membrane-bound organelles in plant cells. Journal of Experimental Botany, 74(10), 2956-2967.
9.Birnbaum, K. D., Otegui, M. S., Bailey-Serres, J., & Rhee, S. Y. (2022). The Plant Cell Atlas: focusing new technologies on the kingdom that nourishes the planet. Plant physiology, 188(2), 675-679.
10.Bittner, A., Cieśla, A., Gruden, K., Lukan, T., Mahmud, S., Teige, M., ... & Wurzinger, B. (2022). Organelles and phytohormones: a network of interactions in plant stress responses. Journal of Experimental Botany, 73(21), 7165-7181.
11.Bulut, M., Karakas, E., & Fernie, A. R. (2025). Metabolic responses to multi-stress: An update. Plant Stress, 15, 100729.
12.Chadee, A., Alber, N. A., Dahal, K., & Vanlerberghe, G. C. (2021). The complementary roles of chloroplast cyclic electron transport and mitochondrial alternative oxidase to ensure photosynthetic performance. Frontiers in Plant Science, 12, 748204.
13.Duckney, P. J., Wang, P., & Hussey, P. J. (2025). Plant NETWORKED and VAP27 proteins work in complexes to regulate membrane-based functions. Contact, 8, 25152564251342533.
14.Fernie, A. R., & Bauwe, H. (2020). Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway. The Plant Journal, 102(4), 666-677.
15.Foyer, C. H., & Hanke, G. (2022). ROS production and signalling in chloroplasts: cornerstones and evolving concepts. The Plant Journal, 111(3), 642-661.
16.Fu, Y., Li, X., Fan, B., Zhu, C., & Chen, Z. (2022). Chloroplasts protein quality control and turnover: a multitude of mechanisms. International Journal of Molecular Sciences, 23(14), 7760.
17.Fuchs, P., Bohle, F., Lichtenauer, S., Ugalde, J. M., Feitosa Araujo, E., Mansuroglu, B., ... & Schwarzländer, M. (2022). Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity. The Plant Cell, 34(4), 1375-1395.
18.Hameed, A., Ahmed, M. Z., Hussain, T., Aziz, I., Ahmad, N., Gul, B., & Nielsen, B. L. (2021). Effects of salinity stress on chloroplast structure and function. Cells, 10(8), 2023.
19.He, C., Berkowitz, O., Hu, S., Zhao, Y., Qian, K., Shou, H., ... & Wang, Y. (2023). Co-regulation of mitochondrial and chloroplast function: Molecular components and mechanisms. Plant Communications, 4(1).
20.He, C., Liew, L. C., Yin, L., Lewsey, M. G., Whelan, J., & Berkowitz, O. (2022). The retrograde signaling regulator ANAC017 recruits the MKK9–MPK3/6, ethylene, and auxin signaling pathways to balance mitochondrial dysfunction with growth. The Plant Cell, 34(9), 3460-3481.
21.Hoh, D., Froehlich, J. E., & Kramer, D. M. (2024). Redox regulation in chloroplast thylakoid lumen: The pmf changes everything, again. Plant, Cell & Environment, 47(8), 2749-2765.
22.Horn, P. J., & Chapman, K. D. (2024). Imaging plant metabolism in situ. Journal of Experimental Botany, 75(6), 1654-1670.
23.Huercano, C., Moya-Barrientos, M., Cuevas, O., Sanchez-Vera, V., & Ruiz-Lopez, N. (2025). ER–plastid contact sites as molecular crossroads for plastid lipid biosynthesis. BMC biology, 23(1), 139.
24.Igamberdiev, A. U., & Bykova, N. V. (2023). Mitochondria in photosynthetic cells: Coordinating redox control and energy balance. Plant Physiology, 191(4), 2104-2119.
25.Jan, M., Liu, Z., Rochaix, J. D., & Sun, X. (2022). Retrograde and anterograde signaling in the crosstalk between chloroplast and nucleus. Frontiers in Plant Science, 13, 980237.
26.Jayawardhane, J., Cochrane, D. W., Vyas, P., Bykova, N. V., Vanlerberghe, G. C., & Igamberdiev, A. U. (2020). Roles for plant mitochondrial alternative oxidase under normoxia, hypoxia, and reoxygenation conditions. Frontiers in Plant Science, 11, 566.
27.Jiang, Z., van Zanten, M., & Sasidharan, R. (2025). Mechanisms of plant acclimation to multiple abiotic stresses. Communications Biology, 8(1), 655.
28.Kang, B. H., Anderson, C. T., Arimura, S. I., Bayer, E., Bezanilla, M., Botella, M. A., ... & Zolman, B. K. (2022). A glossary of plant cell structures: current insights and future questions. The Plant Cell, 34(1), 10-52.
29.Kavi Kishor, P. B., Suravajhala, P., Rathnagiri, P., & Sreenivasulu, N. (2022). Intriguing role of proline in redox potential conferring high temperature stress tolerance. Frontiers in Plant Science, 13, 867531.
30.Kim, H. U. (2020). Lipid metabolism in plants. Plants, 9(7), 871.
31.Kim, J. S., Mochida, K., & Shinozaki, K. (2022). ER stress and the unfolded protein response: homeostatic regulation coordinate plant survival and growth. Plants, 11(23), 3197.
32.Koenig, A. M., Liu, B., & Hu, J. (2023). Visualizing the dynamics of plant energy organelles. Biochemical Society Transactions, 51(6), 2029-2040.
33.Lee, K., & Kang, H. (2020). Roles of organellar RNA-binding proteins in plant growth, development, and abiotic stress responses. International Journal of Molecular Sciences, 21(12), 4548.
34.León, J., Castillo, M. C., & Gayubas, B. (2021). The hypoxia–reoxygenation stress in plants. Journal of Experimental Botany, 72(16), 5841-5856.
35.Li, T., Xiao, Z., Li, H., Liu, C., Shen, W., & Gao, C. (2020). A combinatorial reporter set to visualize the membrane contact sites between endoplasmic reticulum and other organelles in plant cell. Frontiers in Plant Science, 11, 1280.
36.Liu, X., Quan, W., & Bartels, D. (2022). Stress memory responses and seed priming correlate with drought tolerance in plants: An overview. Planta, 255(2), 45.
37.Liu, Y., Lv, Y., Wei, A., Guo, M., Li, Y., Wang, J., ... & Bao, Y. (2022). Unfolded protein response in balancing plant growth and stress tolerance. Frontiers in Plant Science, 13, 1019414.
38.Man, Y., Zhang, Y., Chen, L., Zhou, J., Bu, Y., Zhang, X., ... & Lin, J. (2024). The VAMP-associated protein VAP27-1 plays a crucial role in plant resistance to ER stress by modulating ER–PM contact architecture in Arabidopsis. Plant Communications, 5(7).
39.Mathur, J., Kunjumon, T. K., Mammone, A., & Mathur, N. (2023). Membrane contacts with the endoplasmic reticulum modulate plastid morphology and behaviour. Frontiers in Plant Science, 14, 1293906.
40.Mielecki, J., Gawroński, P., & Karpiński, S. (2020). Retrograde signaling: understanding the communication between organelles. International Journal of Molecular Sciences, 21(17), 6173.
41.Molina-Moya, E., Rodríguez-González, A., Peláez-Vico, M. A., Sandalio, L. M., & Romero-Puertas, M. C. (2025). Peroxisomal-dependent signalling and dynamics modulate plant stress responses: reactive oxygen and nitrogen species as key molecules. Journal of Experimental Botany, 76(13), 3706-3721.
42.Muhammad, I., Shalmani, A., Ali, M., Yang, Q. H., Ahmad, H., & Li, F. B. (2021). Mechanisms regulating the dynamics of photosynthesis under abiotic stresses. Frontiers in Plant Science, 11, 615942.
43.Muñoz, P., & Munné-Bosch, S. (2020). Oxylipins in plastidial retrograde signaling. Redox Biology, 37, 101717.
44.Narra, M., Nakazato, I., Polley, B., Arimura, S. I., Woronuk, G. N., & Bhowmik, P. K. (2025). Recent trends and advances in chloroplast engineering and transformation methods. Frontiers in Plant Science, 16, 1526578.
45.Niu, Q., Zhao, L., Dang, Y., Guo, R., Deng, K., & Xiao, L. (2025). Bryophyte ELIPs as evolutionary guardians: engineering chloroplast resilience and ABA‐enhanced drought tolerance in crops. Plant, Cell & Environment, 48(11), 7948-7960.
46.Otegui, M. S., Steelheart, C., Ma, W., Ma, J., Kang, B. H., De Medina Hernandez, V. S., ... & Nishimura, M. (2024). Vacuolar degradation of plant organelles. The Plant Cell, 36(9), 3036-3056.
47.Page, M. T., Garcia-Becerra, T., Smith, A. G., & Terry, M. J. (2020). Overexpression of chloroplast-targeted ferrochelatase 1 results in a genomes uncoupled chloroplast-to-nucleus retrograde signalling phenotype. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1801), 20190401.
48.Renna, L., Stefano, G., Puggioni, M. P., Kim, S. J., Lavell, A., Froehlich, J. E., ... & Brandizzi, F. (2024). ER-associated VAP27-1 and VAP27-3 proteins functionally link the lipid-binding ORP2A at the ER-chloroplast contact sites. Nature Communications, 15(1), 6008.
49.Resentini, F., Ruberti, C., Grenzi, M., Bonza, M. C., & Costa, A. (2021). The signatures of organellar calcium. Plant Physiology, 187(4), 1985-2004.
50.Richter, A. S., Nägele, T., Grimm, B., Kaufmann, K., Schroda, M., Leister, D., & Kleine, T. (2023). Retrograde signaling in plants: A critical review focusing on the GUN pathway and beyond. Plant Communications, 4(1).
51.Richter, A. S., Tohge, T., Fernie, A. R., & Grimm, B. (2020). The genomes uncoupled-dependent signalling pathway coordinates plastid biogenesis with the synthesis of anthocyanins. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1801), 20190403.
52.Ruiz-Lopez, N., Pérez-Sancho, J., Del Valle, A. E., Haslam, R. P., Vanneste, S., Catalá, R., ... & Botella, M. A. (2021). Synaptotagmins at the endoplasmic reticulum–plasma membrane contact sites maintain diacylglycerol homeostasis during abiotic stress. The Plant Cell, 33(7), 2431-2453.
53.Sadoine, M., Ishikawa, Y., Kleist, T. J., Wudick, M. M., Nakamura, M., Grossmann, G., ... & Ho, C. H. (2021). Designs, applications, and limitations of genetically encoded fluorescent sensors to explore plant biology. Plant Physiology, 187(2), 485-503.
54.Sandalio, L. M., Peláez-Vico, M. A., Molina-Moya, E., & Romero-Puertas, M. C. (2021). Peroxisomes as redox-signaling nodes in intracellular communication and stress responses. Plant Physiology, 186(1), 22-35.
55.Selinski, J., Frings, S., & Schmidt‐Schippers, R. (2024). Perception and processing of stress signals by plant mitochondria. The Plant Journal, 120(6), 2337-2355.
56.Sharma, P., Lakra, N., Goyal, A., Ahlawat, Y. K., Zaid, A., & Siddique, K. H. (2023). Drought and heat stress mediated activation of lipid signaling in plants: a critical review. Frontiers in Plant Science, 14, 1216835.
57.Shimizu, T., & Masuda, T. (2021). The role of tetrapyrrole-and GUN1-dependent signaling on chloroplast biogenesis. Plants, 10(2), 196.
58.Song, Y., Feng, L., Alyafei, M. A. M., Jaleel, A., & Ren, M. (2021). Function of chloroplasts in plant stress responses. International Journal of Molecular Sciences, 22(24), 13464.
59.Suzuki, N. (2023). Fine tuning of ROS, redox and energy regulatory systems associated with the functions of chloroplasts and mitochondria in plants under heat stress. International Journal of Molecular Sciences, 24(2), 1356.
60.Tadini, L., Jeran, N., & Pesaresi, P. (2020). GUN1 and plastid RNA metabolism: learning from genetics. Cells, 9(10), 2307.
61.Tang, H., & Zhu, H. (2022). Specific changes in morphology and dynamics of plant mitochondria under abiotic stress. Horticulturae, 9(1), 11.
62.Unal, D., García-Caparrós, P., Kumar, V., & Dietz, K. J. (2020). Chloroplast-associated molecular patterns as concept for fine-tuned operational retrograde signalling. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1801), 20190443.
63.Van Aken, O. (2021). Mitochondrial redox systems as central hubs in plant metabolism and signaling. Plant Physiology, 186(1), 36-52.
64.van Veen, E., Küpers, J. J., & Gommers, C. M. (2025). Plastids in a pinch: Coordinating stress and developmental responses through retrograde signalling. Plant, Cell & Environment, 48(9), 6897-6911.
65.Wang, Y., Selinski, J., Mao, C., Zhu, Y., Berkowitz, O., & Whelan, J. (2020). Linking mitochondrial and chloroplast retrograde signalling in plants. Philosophical Transactions of the Royal Society B: Biological Sciences, 375(1801), 20190410.
66.Xu, S. L., Shrestha, R., Karunadasa, S. S., & Xie, P. Q. (2023). Proximity labeling in plants. Annual review of plant biology, 74(1), 285-312.
67.Xu, Y., & Fu, X. (2022). Reprogramming of plant central metabolism in response to abiotic stresses: A metabolomics view. International journal of molecular sciences, 23(10), 5716.
68.Yang, X., Wen, Z., Zhang, D., Li, Z., Li, D., Nagalakshmi, U., ... & Zhang, Y. (2021). Proximity labeling: an emerging tool for probing in planta molecular interactions. Plant communications, 2(2).
69.Ye, H., Ji, C., Guo, R., & Jiang, L. (2020). Membrane contact sites and organelles interaction in plant autophagy. Frontiers in Plant Science, 11, 477.
70.Yoshida, K., & Hisabori, T. (2023). Current insights into the redox regulation network in plant chloroplasts. Plant and Cell Physiology, 64(7), 704-715.
71.Zeng, C., Jia, T., Gu, T., Su, J., & Hu, X. (2021). Progress in research on the mechanisms underlying chloroplast-involved heat tolerance in plants. Genes, 12(9), 1343.
72.Zhang, M., Ming, Y., Wang, H. B., & Jin, H. L. (2024). Strategies for adaptation to high light in plants. Abiotech, 5(3), 381-393.
73.Zhang, Y., Zhang, A., Li, X., & Lu, C. (2020). The role of chloroplast gene expression in plant responses to environmental stress. International Journal of Molecular Sciences, 21(17), 6082.
74.Zhu, Y., Narsai, R., He, C., Wang, Y., Berkowitz, O., Whelan, J., & Liew, L. C. (2023). Coordinated regulation of the mitochondrial retrograde response by circadian clock regulators and ANAC017. Plant Communications, 4(1).
75.Zhuang, X., Li, R., & Jiang, L. (2024). A century journey of organelles research in the plant endomembrane system. The Plant Cell, 36(5), 1312-1333.
Published
2026-08-25
How to Cite
Priya R. Nair, Arjun S. Menon, & Kavya P. Rao. (2026). INTERORGANELLE COMMUNICATION IN PLANT STRESS ADAPTATION: MEMBRANE CONTACT SITES, RETROGRADE SIGNALING, AND METABOLIC REPROGRAMMING. IJRDO - JOURNAL OF BIOLOGICAL SCIENCE, 12(3), 21-41. https://doi.org/10.69980/bs.v12i3.6811