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SWEET endo-mutualism with plant roots: Understanding the link between nutrient transport and calcium signaling in plant and Piriformospora indica interaction

Dr. Abhimanyu Jogawat, DBT-MK Bhan-Young Researcher Fellowship, National Institute of Plant Genome Research, New Delhi

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Location : Online
Abstract: Piriformospora indica is a vast host range root endo-mutualist which is even capable of colonizing the roots of non-mycorrhizal Arabidopsis. It stimulates growth as well as stress tolerance of host plant by inducing osmolytes, secondary metabolites and phytohormones (Jogawat et al., 2013, Gahlot et al., 2015 and Kundu et al., 2022). It enhances salinity tolerance of plant and its osmoregulator mitogen activated kinase, PiHOG1 plays crucial role in this process (Jogawat et al., 2013, 16). P. indica transports nutrients such as sulphate and iron to plant roots via its transporters PiSulT and PiFTR, respectively (Narayan et al., 2021 and Verma et al., 2022). P. indica cell wall extract induces cyclic nucleotide gated calcium channels (CNGCs) in plant roots. CNGC19 acts as early gatekeeper and maintains homeostasis of growth and defense during P. indica interaction as its loss-of-function mutant shows plant growth diminution (Jogawat et al., 2020). Central to this symbiosis is the distribution of sugars between the two symbionts and the maintenance of sugar homeostasis. The fungus-derived symbiotic signal mainly cellotriose (CT) stimulates the host immunity by activating systemic defense responses.

Being a glucose oligomer, CT might play a crucial role in linking Ca2+ -dependent immunity signaling and sugar homeostasis. The aim of my present study is to investigate whether Sugar Will Eventually be Exported Transporters (SWEETs) transporters play a role in CT transport or CT-regulated symbiotic/immunity signaling in P. indica-Arabidopsis interaction. We hypothesized that SWEETs are potential candidates which might play dual role in transporting sugars to fungus or transport CT to initiate CT-mediated responses. Our GC/MS and ICPM analyses show that P. indica alters levels of different sugars and elements in colonized plants. Further, time course expression profiling of SWEET genes reveals that SWEETs are induced by P. indica and CT-treatment. We studied loss-of-function mutants of SWEET11 and SWEET12 to identify their functional importance in growth promotion response. The mutants of sweet11 show reduced levels of root colonization, no root growth promotion, and induced defense during co-cultivation whereas sweet12 mutants show increased colonization, reduced growth promotion and reduced defense. Our further analyses revealed interaction of SWEET11 and SWEET12 via their C-terminals. In downstream, SWEET12-C-terminal interacts with SnRK2.8 to trigger defense responses. In conclusion, P. indica or CT modulates the level of sugars and the expression of SWEETs which may affect growth and defense homeostasis of this root endo-mutualism. In depth analysis of the SWEETs’ link between sugar transport and CT-mediated signaling would reveal more insights about the role of SWEETs in growth and defense trade off during P. indica colonization.

References:
1. Kundu, A., Mishra, S., Kundu, P., Jogawat, A. and Vadassery, J. (2022) Piriformospora indica recruits host-derived putrescine for growth promotion in plants. Plant Physiology, 188 (4): 2289-2307. ISSN 2662-2548.

2. Verma, N., Narayan, O.P., Prasad, D., Jogawat, A., Panwar, S.L., Dua, M. and Johri, A.K. (2022). Functional characterization of a high‐affinity iron transporter (PiFTR) from the endophytic fungus Piriformospora indica and its role in plant growth and development. Environmental Microbiology, 24 (2): 689-706. ISSN 1462-2920.

3. Narayan, O.P., Verma, N., Jogawat, A., Dua, M. and Johri, A.K. (2021) Sulfur transfer from the endophytic fungus Serendipita indica improves maize growth and requires the sulfate transporter SiSulT. The Plant Cell, 33 (4) 1268-1285. ISSN 1532298X.

4. Jogawat, A., Meena, M.K., Kundu, A., Varma, M. and Vadassery, J. (2020) Calcium channel CNGC19 mediates basal defense signaling to regulate colonization by Piriformospora indica in Arabidopsis roots. Journal of Experimental Botany, 71(9), 2752-2768. ISSN 0022-0957

5. Jogawat, A., Vadassery, J., Verma, N., Oelmüller, R., Dua, M. and Johri, A.K. (2016). PiHOG1, a stress regulator MAP kinase from the root endophyte fungus Piriformospora indica, confers salinity stress tolerance in rice plants. Scientific Reports 6:36765. ISSN No. 2045-2322

6. Gahlot, S., Joshi, A., Singh, P., Tuteja, R., Dua, M., Jogawat, A., Kumar, M., Dayaman, V., Raj, S., Johri, A.K. and Tuteja, N. (2015) Isolation of genes conferring salt tolerance from Piriformospora indica by random over-expression in Escherichia coli. World Journal of Microbiology and Biotechnology 31(8): 1195-1209. ISSN No. 0959-3993.

7. Jogawat, A., Saha, S., Bakshi, M., Dayaman, V., Kumar, M., Dua, M., Varma, A., Oelmüller, R., Tuteja, N. and Johri, A.K. (2013) Piriformospora indica Rescues Growth Diminution of Rice seedlings during High Salt Stress. Plant Signaling & Behavior 9.1: e26891. ISSN No. 15592316

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