Staff profile

Research Interests

Plant diseases are major limiting factors of worldwide agriculture. Understanding the mechanisms by which pathogens invade plants and the means by which plant perceive the invasion is very important to developing novel control strategies in the future. The control of protein degradation through the ubiquitin-proteasome system (UPS) is a central modifier of signaling in animals and plants. An emerging paradigm in biology is the pathogen mediated targeting of the UPS to suppress host immunity but how pathogens achieve this is not known.

Our group has identified regulatory factors of host UPS that could act as targets for defence suppression by plant pathogens. Using Arabidopsis, tobacco and tomato as model hosts my laboratory employs a cross disciplinary approach including genetic, molecular and biochemical techniques to identify components that are specifically Ubiquitinated by bacterial and fungal pathogens to undermine plant immunity. 

In recent years another class of ubiquitin-related polypeptide tags called small ubiquitin-like modifiers (SUMO) has emerged as a very influential regulator of stress signalling in plants and animals. Nearly all crops are highly susceptible to drought, heat stress and salinity. Our work on post-translational modification of proteins has shown that specific signalling proteins are SUMOylated as part of plant survival strategy during drought, heat and high salinity. We have developed experimental methods to specifically quantify and identify SUMOylated and Ubiquitinated proteins in plants. Understanding how protein modification is regulated will have huge implications for agriculture, as this knowledge will be crucial for generating stress resistant crops. 

Lab Members:

Postdocs:

Dr. Cunjin Zhang

Dr. Beatriz Orosa

Dr. Anjil Srivastava

Dr. Vivek Verma

Phd students:

Charlotte Walsh

Gary Yates

Linda Millyard

Alberto Campanaro

Jack Lee

 

Journal Article

• Eckardt, N. A., Genschik, P., Jiang, L., Li, X., Otegui, M. S., Sadanandom, A., Spoel, S., van Wijk, K. J., & Weijers, D. (online). Focus on proteolysis. The Plant Cell, https://doi.org/10.1093/plcell/koae182
• Ghosh, S., Mellado Sanchez, M., Sue-Ob, K., Roy, D., Jones, A., Blazquez, M. A., & Sadanandom, A. (2024). Charting the evolutionary path of the SUMO modification system in plants reveals molecular hardwiring of development to stress adaptation. The Plant Cell, 36(9), 3131-3144. https://doi.org/10.1093/plcell/koae192
• Lakmes, A., Jhar, A., Sadanandom, A., Brennan, A. C., & Kahriman, A. (2024). Inheritance of Resistance to Chickpea Fusarium Wilt Disease ( Fusarium oxysporum f. sp. ciceris Race 2) in a Wide-Cross Cicer arietinum × Cicer reticulatum Mapping Family. Genes, 15(6), Article 819. https://doi.org/10.3390/genes15060819
• Sureshkumar, S., Bandaranayake, C., Lv, J., Dent, C. I., Bhagat, P. K., Mukherjee, S., Sarwade, R., Atri, C., York, H. M., Tamizhselvan, P., Shamaya, N., Folini, G., Bergey, B. G., Yadav, A. S., Kumar, S., Grummisch, O. S., Saini, P., Yadav, R. K., Arumugam, S., Rosonina, E., …Balasubramanian, S. (2024). SUMO protease FUG1, histone reader AL3 and chromodomain protein LHP1 are integral to repeat expansion-induced gene silencing in Arabidopsis thaliana. Nature Plants, 10, 749-759. https://doi.org/10.1038/s41477-024-01672-5
• Mukkawar, V., Roy, D., Sue-ob, K., Jones, A., Zhang, C., Kumar Bhagat, P., Kakkunnath, S. M., Heuer, S., & Sadanandom, A. (2024). SUMOylation of OsPSTOL1 is essential for regulating phosphate starvation responses in rice and Arabidopsis. Frontiers in Plant Science, 15, Article 1274610. https://doi.org/10.3389/fpls.2024.1274610
• Naranjo-Arcos, M., Srivastava, M., Deligne, F., Bhagat, P. K., Mansi, M., Sadanandom, A., & Vert, G. (2023). SUMO/deSUMOylation of the BRI1 brassinosteroid receptor modulates plant growth responses to temperature. Proceedings of the National Academy of Sciences, 120(4), Article 2217255120. https://doi.org/10.1073/pnas.2217255120
• Srivastava, M., Srivastava, A. K., Roy, D., Mansi, M., Gough, C., Bhagat, P. K., Zhang, C., & Sadanandom, A. (2022). The conjugation of SUMO to the transcription factor MYC2 functions in blue light-mediated seedling development in Arabidopsis. The Plant Cell, 34(8), 2892-2906. https://doi.org/10.1093/plcell/koac142
• Clark, L., Sue-Ob, K., Mukkawar, V., Jones, A., & Sadanandom, A. (2022). Understanding SUMO-mediated adaptive responses in plants to improve crop productivity. Essays in Biochemistry, 66(2), 155-168. https://doi.org/10.1042/ebc20210068
• Campanaro, A., Srivastava, A., Zhang, C., Lee, J., Millyard, L., Gatehouse, A., Byrne, E., & Sadanandom, A. (2021). TaWRKY10 transcription factor is a novel Jasmonic Acid signalling regulator involved in immunity against Septoria tritici blotch disease in wheat. Plant Pathology, 70(6), 1397-1408. https://doi.org/10.1111/ppa.13388
• Verma, V., Srivastava, A. K., Gough, C., Campanaro, A., Srivastava, M., Morrell, R., Joyce, J., Bailey, M., Zhang, C., Krysan, P. J., & Sadanandom, A. (2021). SUMO enables substrate selectivity by mitogen-activated protein kinases to regulate immunity in plants. Proceedings of the National Academy of Sciences, 118(10), Article e2021351118. https://doi.org/10.1073/pnas.2021351118
• Roy, D., & Sadanandom, A. (2021). SUMO mediated regulation of transcription factors as a mechanism for transducing environmental cues into cellular signaling in plants. Cellular and Molecular Life Sciences, 78(6), 2641-2664. https://doi.org/10.1007/s00018-020-03723-4
• Dong, Y., Majda, M., Šimura, J., Horvath, R., Srivastava, A. K., Łangowski, Ł., Eldridge, T., Stacey, N., Slotte, T., Sadanandom, A., Ljung, K., Smith, R. S., & Østergaard, L. (2020). HEARTBREAK Controls Post-translational Modification of INDEHISCENT to Regulate Fruit Morphology in Capsella. Current Biology, 30(19), 3880-3888.e5. https://doi.org/10.1016/j.cub.2020.07.055
• Srivastava, M., Srivastava, A. K., Orosa-Puente, B., Campanaro, A., Zhang, C., & Sadanandom, A. (2020). SUMO Conjugation to BZR1 Enables Brassinosteroid Signaling to Integrate Environmental Cues to Shape Plant Growth. Current Biology, 30(8), 1423.e3-1423.e3. https://doi.org/10.1016/j.cub.2020.01.089
• Srivastava, M., Sadanandom, A., & Srivastava, A. K. (2020). Towards understanding the multifaceted role of SUMOylation in plant growth and development. Physiologia Plantarum, 171(1), 77-85. https://doi.org/10.1111/ppl.13204
• Aliaga-Franco, N., Zhang, C., Presa, S., Srivastava, A. K., Granell, A., Alabadí, D., Sadanandom, A., Blázquez, M. A., & Minguet, E. G. (2019). Identification of Transgene-Free CRISPR-Edited Plants of Rice, Tomato, and Arabidopsis by Monitoring DsRED Fluorescence in Dry Seeds. Frontiers in Plant Science, 10, Article 1150. https://doi.org/10.3389/fpls.2019.01150
• Morrell, R., & Sadanandom, A. (2019). Dealing With Stress: A Review of Plant SUMO Proteases. Frontiers in Plant Science, 10, Article 1122. https://doi.org/10.3389/fpls.2019.01122
• Orosa-Puente, B., Leftley, N., von Wangenheim, D., Banda, J., Srivastava, A. K., Hill, K., Truskina, J., Bhosale, R., Morris, E., Srivastava, M., Kümpers, B., Goh, T., Fukaki, H., Vermeer, J. E., Vernoux, T., Dinneny, J. R., French, A. P., Bishopp, A., Sadanandom, A., & Bennett, M. J. (2018). Root branching toward water involves posttranslational modification of transcription factor ARF7. Science, 362(6421), 1407-1410. https://doi.org/10.1126/science.aau3956
• Orosa, B., Yates, G., Verma, V., Srivastava, A. K., Srivastava, M., Campanaro, A., De Vega, D., Fernandes, A., Zhang, C., Lee, J., Bennett, M. J., & Sadanandom, A. (2018). SUMO conjugation to the pattern recognition receptor FLS2 triggers intracellular signalling in plant innate immunity. Nature Communications, 9(1), Article 5185. https://doi.org/10.1038/s41467-018-07696-8
• Srivastava, A. K., Orosa, B., Singh, P., Cummins, I., Walsh, C., Zhang, C., Grant, M., Roberts, M. R., Anand, G. S., Fitches, E., & Sadanandom, A. (2018). SUMO Suppresses the Activity of the Jasmonic Acid Receptor CORONATINE INSENSITIVE1. The Plant Cell, 30(9), 2099-2115. https://doi.org/10.1105/tpc.18.00036
• Castro, P. H., Bachmair, A., Bejarano, E. R., Coupland, G., Lois, L. M., Sadanandom, A., van den Burg, H. A., Vierstra, R. D., & Azevedo, H. (2018). Revised nomenclature and functional overview of the ULP gene family of plant deSUMOylating proteases. Journal of Experimental Botany, 69(19), 4505-4509. https://doi.org/10.1093/jxb/ery301
• De Vega, D., Newton, A. C., & Sadanandom, A. (2018). Post-translational modifications in priming the plant immune system: ripe for exploitation?. FEBS Letters, 592(12), 1929-1936. https://doi.org/10.1002/1873-3468.13076
• Verma, V., Croley, F., & Sadanandom, A. (2018). Fifty shades of SUMO: its role in immunity and at the fulcrum of the growth-defence balance. Molecular Plant Pathology, 19(6), 1537-1544. https://doi.org/10.1111/mpp.12625
• Orosa, B., He, Q., Mesmar, J., Gilroy, E. M., McLellan, H., Yang, C., Craig, A., Bailey, M., Zhang, C., Moore, J. D., Boevink, P. C., Tian, Z., Birch, P. R., & Sadanandom, A. (2017). BTB-BACK Domain Protein POB1 Suppresses Immune Cell Death by Targeting Ubiquitin E3 ligase PUB17 for Degradation. PLoS Genetics, 13(1), Article e1006540. https://doi.org/10.1371/journal.pgen.1006540
• Bailey, M., Srivastava, A., Conti, L., Nelis, S., Zhang, C., Florance, H., Love, A., Milner, J., Napier, R., Grant, M., & Sadanandom, A. (2016). Stability of small ubiquitin-like modifier (SUMO) proteases OVERLY TOLERANT TO SALT1 and -2 modulates salicylic acid signalling and SUMO1/2 conjugation in Arabidopsis thaliana. Journal of Experimental Botany, 67(1), 353-363. https://doi.org/10.1093/jxb/erv468
• Sadanandom, A., Ádám, É., Orosa, B., Viczián, A., Klose, C., Zhang, C., Josse, E., Kozma-Bognár, L., & Nagy, F. (2015). SUMOylation of phytochrome-B negatively regulates light-induced signaling in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, 112(35), 11108-11113. https://doi.org/10.1073/pnas.1415260112
• Domingues, M., Sforça, M., Soprano, A., Lee, J., Campos Brasil de Souza, T. D. A., Cassago, A., Portugal, R., de Mattos Zeri, A., Murakami, M., Sadanandom, A., de Oliveira, P., & Benedetti, C. (2015). Structure and Mechanism of Dimer-Monomer Transition of a Plant Poly(A)-Binding Protein upon RNA Interaction: Insights into Its Poly(A) Tail Assembly. Journal of Molecular Biology, 427(15), 2491-2506. https://doi.org/10.1016/j.jmb.2015.05.017
• He, Q., McLellan, H., Boevink, P., Sadanandom, A., Xie, C., Birch, P., & Tian, Z. (2015). U-box E3 ubiquitin ligase PUB17 acts in the nucleus to promote specific immune pathways triggered by Phytophthora infestans. Journal of Experimental Botany, 66(11), 3189-3199. https://doi.org/10.1093/jxb/erv128
• Verma, V., Sivaraman, J., Srivastava, A., Sadanandom, A., & Kumar, P. (2015). Destabilization of interaction between cytokinin signaling intermediates AHP1 and ARR4 modulates Arabidopsis development. New Phytologist, 206(2), 726-737. https://doi.org/10.1111/nph.13297
• Lee, J., Orosa, B., Millyard, L., Edwards, M., Kanyuka, K., Gatehouse, A., Rudd, J., Hammond-Kosack, K., Pain, N., & Sadanandom, A. (2015). Functional analysis of a Wheat Homeodomain protein, TaR1, reveals that host chromatin remodelling influences the dynamics of the switch to necrotrophic growth in the phytopathogenic fungus Zymoseptoria tritici. New Phytologist, 206(2), 598-605. https://doi.org/10.1111/nph.13323
• Nelis, S., Conti, L., Zhang, C., & Sadanandom, A. (2015). A functional Small Ubiquitin-like Modifier (SUMO) interacting motif (SIM) in the gibberellin hormone receptor GID1 is conserved in cereal crops and disrupting this motif does not abolish hormone dependency of the DELLA-GID1 interaction. Plant Signaling & Behavior, 10(2), https://doi.org/10.4161/15592324.2014.987528
• Walsh, C., & Sadanandom, A. (2014). Ubiquitin chain topology in plant cell signaling: a new facet to an evergreen story. Frontiers in Plant Science, 5, https://doi.org/10.3389/fpls.2014.00122
• Conti, L., Nelis, S., Zhang, C., Woodcock, A., Swarup, R., Galbiati, M., Tonelli, C., Napier, R., Hedden, P., Bennett, M., & Sadanandom, A. (2014). Small Ubiquitin-like Modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Developmental Cell, 28(1), 102-110. https://doi.org/10.1016/j.devcel.2013.12.004
• Laird, J., McInally, C., Carr, C., Doddiah, S., Yates, G., Chrysanthou, E., Khattab, A., Love, A., Geri, C., Sadanandom, A., Smith, B., Kobayashi, K., & Milner, J. (2013). Identification of the domains of cauliflower mosaic virus protein P6 responsible for suppression of RNA silencing and salicylic acid signalling. Journal of General Virology, 94(12), 2777-2789. https://doi.org/10.1099/vir.0.057729-0
• Yates, G., & Sadanandom, A. (2013). Ubiquitination in plant nutrient utilization. Frontiers in Plant Science, 4, https://doi.org/10.3389/fpls.2013.00452
• Love, A., Geri, C., Laird, J., Carr, C., Yun, B., Loake, G., Tada, Y., Sadanandom, A., & Milner, J. (2012). Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS ONE, 7(10), https://doi.org/10.1371/journal.pone.0047535
• Sadanandom, A., Bailey, M., Ewan, R., Lee, J., & Nelis, S. (2012). The ubiquitin-proteasome system: central modifier of plant signalling. New Phytologist, 196(1), 13-28. https://doi.org/10.1111/j.1469-8137.2012.04266.x
• Gilroy, E., Taylor, R., Hein, I., Boevink, P., Sadanandom, A., & Birch, P. (2011). CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytologist, 190(3), 653-666. https://doi.org/10.1111/j.1469-8137.2011.03643.x
• regulators of plant immunity. New Phytologist, 191(1), 92-106. https://doi.org/10.1111/j.1469-8137.2011.03672.x
• Sadanandom, A., & Napier, R. (2010). Biosensors in plants. Current Opinion in Plant Biology, 13(6), 736-743. https://doi.org/10.1016/j.pbi.2010.08.010
• Bos, J., Armstrong, M., Gilroy, E., Boevink, P., Hein, I., Taylor, R., Tian, Z., Engelhardt, S., Vetukuri, R., Harrower, B., Dixelius, C., Bryan, G., Sadanandom, A., Whisson, S., Kamoun, S., & Birch, P. (2010). Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proceedings of the National Academy of Sciences, 107(21), 9909-9914. https://doi.org/10.1073/pnas.0914408107
• Morris, K., Thornber, S., Codrai, L., Richardson, C., Craig, A., Sadanandom, A., Thomas, B., & Jackson, S. (2010). DAY NEUTRAL FLOWERING Represses CONSTANS to Prevent Arabidopsis Flowering Early in Short Days. The Plant Cell, 22(4), 1118-1128. https://doi.org/10.1105/tpc.109.066605
• Haas, B., Kamoun, S., Zody, M., Jiang, R., Handsaker, R., Cano, L., Grabherr, M., Kodira, C., Raffaele, S., Torto-Alalibo, T., Bozkurt, T., Ah-Fong, A., Alvarado, L., Anderson, V., Armstrong, M., Avrova, A., Baxter, L., Beynon, J., Boevink, P., Bollmann, S., …Nusbaum, C. (2009). Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature, 461(7262), 393-398. https://doi.org/10.1038/nature08358
• Love, A., Milner, J., & Sadanandom, A. (2009). Response to Cacas and Diamond: Is the autophagy machinery an executioner of programmed cell death in plants?. Trends in Plant Science, 14(6), 300-301. https://doi.org/10.1016/j.tplants.2009.02.009
• Sadanandom, A. (2009). Preface. Journal of Experimental Botany, 60(4), 1083-1083. https://doi.org/10.1093/jxb/erp064
• Birch, P., Armstrong, M., Bos, J., Boevink, P., Gilroy, E., Taylor, R., Wawra, S., Pritchard, L., Conti, L., Ewan, R., Whisson, S., van West, P., Sadanandom, A., & Kamoun, S. (2009). Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. Journal of Experimental Botany, 60(4), 1133-1140. https://doi.org/10.1093/jxb/ern353
• Craig, A., Ewan, R., Mesmar, J., Gudipati, V., & Sadanandom, A. (2009). E3 ubiquitin ligases and plant innate immunity. Journal of Experimental Botany, 60(4), 1123-1132. https://doi.org/10.1093/jxb/erp059
• Conti, L., Kioumourtzoglou, D., Donnell, E. O., Dominy, P., & Sadanandom, A. (2009). OTS1 and OTS2 SUMO proteases link plant development and survival under salt stress. Plant Signaling & Behavior, 4(3), https://doi.org/10.4161/psb.4.3.7867
• Love, A., Milner, J., & Sadanandom, A. (2008). Timing is everything: regulatory overlap in plant cell death. Trends in Plant Science, 13(11), 589-595. https://doi.org/10.1016/j.tplants.2008.08.006
• Conti, L., Price, G., O'Donnell, E., Schwessinger, B., Dominy, P., & Sadanandom, A. (2008). Small Ubiquitin-Like Modifier Proteases OVERLY TOLERANT TO SALT1 and-2 Regulate Salt Stress Responses in Arabidopsis. The Plant Cell, 20(10), 2894-2908. https://doi.org/10.1105/tpc.108.058669
• Love, A., Geri, C., Laird, J., Yuri, B., Loake, G., Sadanandom, A., & Milner, J. (2008). An effector protein encoded by cauliflower mosaic virus inhibits SA-dependent defence responses in Arabidopsis via an NPR1-dependent mechanism. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 150(3), S193-S193. https://doi.org/10.1016/j.cbpa.2008.04.528
• Sadanandom, A., Mesmar, J., Yang, C., Ewan, R., Carr, C., & O' Donnell, E. (2008). The cell death regulator AtPUB17 directly interacts with the BTB/POZ domain transcriptional repressor, AtBTB1 to control disease resistance in plants. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 150(3), S178-S179. https://doi.org/10.1016/j.cbpa.2008.04.475
• Love, A., Laird, J., Holt, J., Hamilton, A., Sadanandom, A., & Milner, J. (2007). Cauliflower mosaic virus protein P6 is a suppressor of RNA silencing. Journal of General Virology, 88, 3439-3444. https://doi.org/10.1099/vir.0.83090-0
• Sadanandom, A. (2007). The U-box protein AtPUB17 is a functional ortholog of NtACRE276 and its E3 ubiquitin ligase activity is required for plant cell death and defence. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 146(4), S203-S203. https://doi.org/10.1016/j.cbpa.2007.01.450
• Conti, L., Donnel, E., Price, J., Love, A., Dominy, P., & Sadanandom, A. (2007). SUMO proteases regulate ROS production in Arabidopsis. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology, 146(4), S260-S260. https://doi.org/10.1016/j.cbpa.2007.01.656
• Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noel, L., Sadanandom, A., Casais, C., Parker, J., & Shirasu, K. (2006). Role of SGT1 in resistance protein accumulation in plant immunity. The EMBO Journal, 25(9), 2007-2016. https://doi.org/10.1038/sj.emboj.7601084
• Yang, C., Gonzalez-Lamothe, R., Ewan, R., Rowland, O., Yoshioka, H., Shenton, M., Ye, H., O'Donnell, E., Jones, J., & Sadanandom, A. (2006). The E3 ubiquitin ligase activity of Arabidopsis PLANT U-BOX17 and its functional tobacco homolog ACRE276 are required for cell death and defense. The Plant Cell, 18(4), 1084-1098. https://doi.org/10.1105/tpc.105.039198
• Sadanandom, A., Findlay, K., Doonan, J., Schulze-Lefert, P., & Shirasu, K. (2004). CHPA, a cysteine- and histidine-rich-domain-containing protein, contributes to maintenance of the diploid state in Aspergillus nidulans. Eukaryotic cell, 3(4), 984-991. https://doi.org/10.1128/ec.3.4.984-991.2004
• Peart, J., Lu, R., Sadanandom, A., Malcuit, I., Moffett, P., Brice, D., Schauser, L., Jaggard, D., Xiao, S., Coleman, M., Dow, M., Jones, J., Shirasu, K., & Baulcombe, D. (2002). Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proceedings of the National Academy of Sciences, 99(16), 10865-10869. https://doi.org/10.1073/pnas.152330599
• Tornero, P., Merritt, P., Sadanandom, A., Shirasu, K., Innes, R., & Dangl, J. (2002). RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. The Plant Cell, 14(5), 1005-1015. https://doi.org/10.1105/tpc.001032
• Muskett, P., Kahn, K., Austin, M., Moisan, L., Sadanandom, A., Shirasu, K., Jones, J., & Parker, J. (2002). Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. The Plant Cell, 14(5), 979-992. https://doi.org/10.1105/tpc.001040
• Azevedo, C., Sadanandom, A., Kitagawa, K., Freialdenhoven, A., Shirasu, K., & Schulze-Lefert, P. (2002). The RAR1 interactor SGT1, an essential component of R gene-triggered disease resistance. Science, 295(5562), 2073-2076
• Sadanandom, A., Poghosyan, Z., Fairbairn, D., & Murphy, D. (2000). Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis. Plant Physiology, 123(1), 255-263
• Sadanandom, A., Piffanelli, P., Knott, T., Robinson, C., Sharpe, A., Lydiate, D., Murphy, D., & Fairbairn, D. (1996). Identification of a peptide methionine sulphoxide reductase gene in an oleosin promoter from Brassica napus. The Plant Journal, 10(2), 235-242