A tomato LATERAL ORGAN BOUNDARIES transcription factor, SlLOB1, predominantly regulates cell wall and softening components of ripening

Authors: SHI, YANNA - Boyce Thompson Institute; VREBALOV, JULIA - Boyce Thompson Institute; ZHENG, HUI - Zhejiang University; XU, YIMIN - Boyce Thompson Institute; YIN, XUEREN - Zhejiang University; LIU, WENLI - Zhejiang University; LIU, ZIMENG - Zhejiang University; SORENSEN, IBEN - Cornell University; SU, GUANQING - Zhejiang University; MA, QIYUE - Boyce Thompson Institute; EVANICH, DANIEL - Cornell University; ROSE, JOCELYN - Cornell University; FEI, ZHANGJUN - Boyce Thompson Institute; VAN ECK, JOYCE - Boyce Thompson Institute; Thannhauser, Theodore - Ted; CHEN, KUNSONG - Zhejiang University; Giovannoni, James

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/30/2021
Publication Date: 8/17/2021
Citation: Shi, Y., Vrebalov, J., Zheng, H., Xu, Y., Yin, X., Liu, W., Liu, Z., Sorensen, I., Su, G., Ma, Q., Evanich, D., Rose, J., Fei, Z., Van Eck, J., Thannhauser, T.W., Chen, K., Giovannoni, J.J. 2021. A tomato LATERAL ORGAN BOUNDARIES transcription factor, SlLOB1, predominantly regulates cell wall and softening components of ripening. Proceedings of the National Academy of Sciences (PNAS). 118(33):e2102486118. https://doi.org/10.1073/pnas.2102486118.
DOI: https://doi.org/10.1073/pnas.2102486118

Interpretive Summary: Tomato (Solanum lycopersicum) is a widely studied model of fleshy fruit development and ripening. Softening is an important aspect of ripening physiology, as it determines palatability for seed dispersing animals and is a key factor in determining damage and loss in fruit food supply chains. Genotypes inhibited in ripening, early harvest, and controlled atmospheres limiting respiration and ethylene synthesis are deployed to maintain firmness and shelf life, often at the expense of quality. A clearer under- standing of the genetic basis of fruit softening and ripening regulation are essential to optimize shelf life and quality for food and nutritional security. Here we have identified and characterized a novel transcriptional regulator, SlLOB1, that specifically regulates downstream genes mostly related to cell wall loosening and softening. As such, SlLOB1 serves as a genetic target to modify fruit texture without negative effects on desirable aspects of ripening.

Technical Abstract: Fruit softening is a key component of the irreversible ripening program, contributing to the palatability necessary for frugivore-mediated seed dispersal. The underlying textural changes are complex and result from cell wall remodeling and changes in both cell adhesion and turgor. While a number of transcription factors (TFs) that regulate ripening have been identified, these affect most canonical ripening-related physiological processes. Here, we show that a tomato fruit ripening–specific LATERAL ORGAN BOUNDRIES (LOB) TF, SlLOB1, up-regulates a suite of cell wall–associated genes during late maturation and ripening of locule and pericarp tissues. SlLOB1 repression in transgenic fruit impedes softening, while overexpression throughout the plant under the direction of the 35s promoter confers precocious induction of cell wall gene expression and premature softening. Transcript and protein levels of the wall-loosening protein EXPANSIN1 (EXP1) are strongly suppressed in SlLOB1 RNA interference lines, while EXP1 is induced in SlLOB1-overexpressing transgenic leaves and fruit. In contrast to the role of ethylene and previously characterized ripening TFs, which are comprehensive facilitators of ripening phenomena including softening, SlLOB1 participates in a regulatory subcircuit predominant to cell wall dynamics and softening.