Evolution of immune mechanisms in monocots and dicots in response to microbial pathogens and abiotic stressors

M. V. Patyka; S. H. Khablak; T. I. Patyka; L. M. Bondareva; M. M. Dolia; V. M. Spychak; Y. V. Lykholat

doi:10.15421/012531

M. V. Patyka Qufu Normal University, Qufu, China; National University of Life and Environmental Sciences of Ukraine, Kyiv, Ukraine
S. H. Khablak Institute of Food Biotechnology and Genomics of the National Academy of Sciences of Ukraine
T. I. Patyka Qufu Normal University
L. M. Bondareva National University of Life and Environmental Sciences of Ukraine
M. M. Dolia National University of Life and Environmental Sciences of Ukraine
V. M. Spychak Institute of Food Biotechnology and Genomics of the National Academy of Sciences of Ukraine
Y. V. Lykholat Oles Honchar Dnipro National University

Keywords: plant immune evolution, non-specific resistance, Triticum aestivum, Helianthus annuus, ABC transporters, lipid transfer proteins (LTPs), WAK receptors, systemic acquired resistance, localized immune response.

Abstract

An in-depth comparative analysis of the evolutionary features of non-specific immune mechanism formation in mon o cotyledonous ( Triticum aestivum L.) and dicotyledonous ( Helianthus annuus L.) plants has been conducted. The main focus is on the differential role of key protein families – ABC transporters, lipid transfer proteins (LTPs), and wall-associated k i nase receptors (WAKs) – in modulating immune signaling cascades in response to various pathogenic and stress factors. The study demonstrates that winter wheat effectively implements systemic acquired resistance (SAR) mechanisms, particularly through the functioning of ABCG transporters (e.g., Lr34), ensuring long-term, quantitative resistance to a wide range of microbial pathogens. In contrast, sunflower predominantly exhibits a localized immune response (LAR), where ROS signa l ing, activated via WAK receptors, plays a key role, ensuring rapid response to necrotrophic pathogens and abiotic factors. The analysis indicates significant functional divergence of orthologous proteins: in wheat, WAK receptors and LTPs are primarily involved in strengthening physical barriers, whereas in sunflower, WAKs function as primary damage sensors (DAMPs) and activators of local stress pathways, and LTPs participate in signaling processes and membrane stabilization. Different immune strategies correlate with physiological-anatomical features and evolutionary adaptation to dominant p a thogen types. The obtained results underscore the importance of integrating knowledge about the molecular mechanisms of non-specific immunity into breeding programs and biotechnological approaches to create cultivars with enhanced and dur a ble resistance. Unresolved questions, particularly regarding the precise activation mechanisms of WAK receptors, and pro s pects for further research are discussed.

References

Atkinson, N. J., & Urwin, P. E. (2012). The interaction of plant biotic and abiotic stresses: From genes to the field. Journal of Experimental Botany, 63(10), 3523–3543.

Badouin, H., Gouzy, J., Grassa, C. J., Murat, F., Staton, S. E., Cottret, L., Lelandais-Brière, C., Owens, G. L., Carrère, S., Mayjonade, B., Legrand, L., Gill, N., Kane, N. C., Bowers, J. E., Hubner, S., Bellec, A., Bérard, A., Bergès, H., Blanchet, N., … Langlade, N. B. (2017). The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution. Nature, 546(7656), 148–152.

Bazzalo, M. E., Dimarco, P. N., & de la Canal, L. (2019). Sunflower immunity: A tale of defense strategies against pathogens. Planta, 249(4), 975–990.

Bechtold, U., & Field, B. (2018). Molecular mechanisms controlling plant growth during abiotic stress. Journal of Experimental Botany, 69(11), 2753–2758.

Boller, T., & Felix, G. (2009). A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology, 60, 379–406.

Borghi, L., Kang, J., Ko, D., Lee, Y., & Martinoia, E. (2015). The role of ABCG-type ABC transporters in phytohormone transport. Biochemical Society Transactions, 43(5), 924–930.

Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Thomas, L. (2009). MaddenBLAST+: Architecture and applications. BMC Bioinformatics, 10, 421.

Dangl, J. L., Horvath, D. M., & Staskawicz, B. J. (2013). Pivoting the plant immune system from dissection to deployment. Science, 341(6147), 746–751.

Dodds, P. N., & Rathjen, J. P. (2010). Plant immunity: Towards an integrated view of plant–pathogen interactions. Nature Reviews Genetics, 11(8), 539–548.

Harrison, P. W., Amode, M. R., Austine-Orimoloye, O., Azov, A. G., Barba, M., Barnes, I., ... & Yates, A. D. (2024). Ensembl 2024. Nucleic Acids Research, 52(D1), D891–D899.

Harvey, C.-L., van den Berg, N., & Swart, V. (2024). A systematic review of wall-associated kinase/kinase-like (WAK/WAKL) characterizations across plant species and a proposed strategy for increased consistency. Frontiers in Plant Science, 15, 1467148.

Herold, L., Ordon, J., Hua, C., Kohorn, B. D., Nürnberger, T., DeFalco, T. A., & Zipfel, C. (2025). Arabidopsis wall-associated kinases are not required for oligogalacturonide-induced signaling and immunity. Plant Cell, 37(1), koae317.

Huang, K., Jahani, M., Gouzy, J., Legendre, A., Carrere, S., Lázaro-Guevara, J. M., ... & Rieseberg, L. H. (2023). The genomics of linkage drag in inbred lines of sunflower. Proceedings of the National Academy of Sciences, 120(14), e2205783119.

Ivanova, T., & Patyka, M. (2023). Analysis of phylogenetic variation the dominant microorganisms species of Pseudomonas fluorescens revealed from mushrooms. Annals of the University of Oradea, Fascicle Biology, 30(2), 99–104.

Jones, J. D., & Dangl, J. L. (2006). The plant immune system. Nature, 444(7117), 323–329.

Kang, J., Hwang, J.-U., Lee, M., Kim, Y.-Y., Assmann, S. M., Martinoia, E., & Lee, Y. (2010). PDR-type ABC transporter mediates cellular uptake of the phytohormone abscisic acid. Proceedings of the National Academy of Sciences, 107(5), 2355–2360.

Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., & Sternberg, M. J. E. (2015). The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10(6), 845–858.

Kohorn, B. D., & Kohorn, S. L. (2012). The cell wall-associated kinases, WAKs, as pectin receptors. AoB Plants, 2012, pls004.

Kourelis, J., & van der Hoorn, R. A. (2018). Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. The Plant Cell, 30(2), 285–299.

Koyama, R., Suzuki, A., Ohnishi, K., Hikichi, Y., & Kiba, A. (2025). Lipid transfer protein VAS inhibits the hypersensitive response via reactive oxygen species signaling in Nicotiana benthamiana. Journal of Experimental Botany, 76(4), 1285–1299.

Krattinger, S. G., Lagudah, E. S., Spielmeyer, W., Singh, R. P., Huerta-Espino, J., McFadden, H., ... & Keller, B. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science, 323(5919), 1360–1363.

Mistry, J., Chuguransky, S., Williams, L., Qureshi, M., Salazar, G. A., Sonnhammer, E. L. L., Tosatto, S. C. E., Paladin, L., Raj, S., Richardson, L. J., Finn, R. D., & Bateman, A. (2020). Pfam: The protein families database in 2021. Nucleic Acids Research, 49(D1), D412–D419.

Osuna-Cruz, C. M., Paytuvi-Gallart, A., Di Donato, A., Sundesha, V., Andolfo, G., Aiese Cigliano, R., ... & Ercolano, M. R. (2018). PRGdb 3.0: A comprehensive platform for prediction and analysis of plant disease resistance genes. Nucleic Acids Research, 46(D1), D1197–D1201.

Poland, J. A., Balint-Kurti, P. J., Wisser, R. J., Pratt, R. C., & Nelson, R. J. (2009). Shades of gray: The world of quantitative disease resistance. Trends in Plant Science, 14(1), 21–29.

Ramírez-González, R. H., Borrill, P., Lang, D., Harrington, S. A., Brinton, J., Venturini, L., ... & Uauy, C. (2018). The transcriptional landscape of polyploid wheat. Science, 361(6403), eaar6089.

Salcedo, G., Sánchez-Monge, R., Barber, D., & Diaz-Perales, A. (2007). Plant non-specific lipid transfer proteins: An interface between plant defence and human allergy. Biochimica et Biophysica Acta – Molecular and Cell Biology of Lipids, 1771(6), 781–791.

Smetanska, I., Tonkha, O., Patyka, T., Hunaefi, D., Mamdouh, D., Patyka, M., ... & Omelian, A. (2021). The influence of yeast extract and jasmonic acid on phenolic acids content of in vitro hairy root cultures of Orthosiphon aristatus. Potravinarstvo, 15(1), 1–8.

UniProt: the Universal Protein Knowledgebase in 2023 (2023). Nucleic Acids Research, 51(1), 523–531.

Velásquez, A. C., Castroverde, C. D., & He, S. Y. (2018). Plant–pathogen warfare under climate change. Current Biology, 28(10), 619–634.

Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015). The I-TASSER Suite: Protein structure and function prediction. Nature Methods, 12(1), 7–8.