COI1 F-box proteins regulate DELLA protein levels, growth, and photosynthetic efficiency in maize

Authors: FEIZ, LEILA - Boyce Thompson Institute; SHYU, CHRISTINE - Bayer Cropscience; WU, SHAN - Boyce Thompson Institute; AHERN, KEVIN - Boyce Thompson Institute; GULL, IRAM - Boyce Thompson Institute; WONG, YING - (NCE, CECR)networks Of Centres Of Exellence Of Canada, Centres Of Excellence For Commercilization A; ARTYMOWICZ, CAROLINE - Boyce Thompson Institute; Pineros, Miguel; FEI, ZHANGJUN - Cornell University; BRUTNELL, THOMAS - Biotechnology Research And Development Corporation (BRDC); JANDER, GEORG - Boyce Thompson Institute

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/23/2024
Publication Date: 5/27/2024
Citation: Feiz, L., Shyu, C., Wu, S., Ahern, K., Gull, I., Wong, Y., Artymowicz, C., Pineros, M., Fei, Z., Brutnell, T., Jander, G. 2024. COI1 F-box proteins regulate DELLA protein levels, growth, and photosynthetic efficiency in maize. The Plant Cell. vol 36(9):3237-3259. https://doi.org/10.1093/plcell/koae161.
DOI: https://doi.org/10.1093/plcell/koae161

Interpretive Summary: Jasmonic acid (JA) is a type of plant hormone involved in the regulation of plant resistance to pathogen infection and development in plants, through a signaling pathway involving its binding to nuclear receptors (COI). To understand the roles of COI proteins in maize, functional changes were recorded in mutants losing the function of six different COI members. Most notably, a quadruple mutant of the maize COI1 genes did not affect defense against insect attacks but rather showed a short height and delayed growth, decreased photosynthesis, and nutrient deficiencies, accompanied by increased levels of protein members of the DELLA family. These proteins are known to negatively regulate the plant hormone gibberellin (GA) signaling processes involved in controlling plant growth. Gene expression analysis revealed a novel interplay between the jasmonic acid (JA) and gibberellin (GA) pathways, and the diverse roles of the COI and DELLA proteins in regulating plant growth and defense mechanisms in maize, with COI compensating for growth penalty associated normally with plant defense responses.

Technical Abstract: The F-box protein Coronatine Insensitive (COI) is a receptor for the jasmonic acid signaling pathway in plants. To investigate the functions of the six maize COI proteins (COI1a, COI1b, COI1c, COI1d, COI2a, and COI2b), we made single, double, and quadruple loss-of-function mutants. Double-mutant coi2a coi2b pollen was inviable, and no homozygous mutant plants were obtained. The coi1 quadruple mutant (coi1-4x) exhibited shortened internode lengths, decreased photosynthesis, leaf discoloration, microelement deficiencies, and accumulation of DWARF9, a DELLA-family protein that represses the gibberellic acid signaling pathway. Co-expression of maize COI and DWARF9 genes in Nicotiana benthamiana showed that the COI proteins lead to proteasome-dependent DELLA degradation. Many genes expressed at lower levels in the coi1-4x mutant are normally induced by gibberellic acid. The majority of these genes are predicted to be bundle sheath or mesophyll-enriched including those encoding C4-specific photosynthetic enzymes. Ectopic expression of maize COI genes in N. benthamiana showed that COI2a is fully localized in the nucleus and interacts with maize JAZ proteins, the canonical COI repressor partners. However, maize COI1a and COI1c proteins showed only partial nuclear localization and failed to bind to most of the JAZ proteins tested. These results show divergent functions of the six COI proteins in the regulation of maize growth and defense pathways.