Auxin response and transport during induction of pedicel abscission in tomato

Authors: DONG, XIUFEN - Shenyang Agricultural University; MA, CHAO - China Agricultural University; XU, TAO - Shenyang Agricultural University; REID, MICHAEL - University Of California, Davis; Jiang, Cai-Zhong; LI, TAINLAI - Shenyang Agricultural University

Submitted to: Horticulture Research
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/7/2021
Publication Date: 9/1/2021
Citation: Dong, X., Ma, C., Xu, T., Reid, M., Jiang, C., Li, T. 2021. Auxin response and transport during induction of pedicel abscission in tomato. Horticulture Research. 8. Article 192. https://doi.org/10.1038/s41438-021-00626-8.
DOI: https://doi.org/10.1038/s41438-021-00626-8

Interpretive Summary: Abscission is the process of organ separation and functions a successful strategy to adapt to the surrounding environment in response to growth, developmental and environmental cues. Abscission allows plants to detach nonfunctional or diseased organs, and is also important for continuation of the species through dispersing progeny. The timing of abscission, especially flower and fruit abscission is of interest to agriculture. Breeding of appropriate abscission has successfully solved problems related to the crop yield loss such as grain shattering, cotton bolls shedding, earlier legume dehiscence as well as mechanical harvest in tomato. It has been well-known that the timing of abscission is regulated by the cross-talk of the phytohormones auxin and ethylene. Ethylene plays an important role as a regulator that accelerates abscission. On the other hand, auxin plays a critical role as a brake that inhibits the cell separation process. The continuous polar flow of auxin passing by the abscission zone (AZ) inhibits the abscission. The depletion of auxin initiates abscission by making the AZ sensitive to ethylene. This auxin-related mechanism would inhibit organ shedding when abscission is inappropriate, despite elevated production of ethylene, such as during the ripening of climacteric fruit. These observations demonstrate that the gradient of auxin passing through AZ tissues might play a crucial role of abscission initiation. Interestingly, application of indole-3-acetic acid (IAA), a major auxin source, to the distal site of P. vulgaris leaf explants inhibits abscission process while the IAA treatment on proximal site accelerates separation of AZ. These studies suggest that the proper auxin gradient throughout AZ must be maintained for initiation of the abscission process. Given the important relevance of auxin balance between the distal and proximal site of AZ for organ shedding, it is essential to understand how this auxin gradient is maintained for regulating initiation of abscission process in response to developmental and environmental cues. Environmental cues especially temperature and lights have huge impacts on organ abscission. It has been reported in various plant species that high temperature accelerates reproductive organ abscission. In cotton, day temperatures above 40°C can induce flower abscission. In soybean, flower abscission was found to increase with the elevated temperature treatment in three different soybean varieties, while no significant differences between control and cool temperature treatments. In addition, shading as well as dark treatments induced reproductive organ abscission in several plants. In pepper, shading treatment enhanced flower abscission in several cultivars. In apple, periods of darkness, shading or cloudy weather have been showed to increase fruit abscission leading to early fruit drop. Nineteen days of shading treatment caused 98% of the fruit to abscise. In grape, percentage of fruit sets was reduced by 5 days shading at bloom. However, the mechanisms of high temperature, or dark/low light-induced abscission and whether auxin is involved in these processes are still unknown. Here, we used a DR5::GUS reporter system that provides visual assessment for evaluation of auxin level/response, to investigate dynamics of auxin signal gradient in response to developmental and environmental cues in pedicel AZ of tomato. Our results showed that in tomato pedicel, GUS activity was predominantly detected in the vascular tissues and higher on the distal side than the proximal side of abscission zone (AZ), suggesting the ‘distal-to-proximal’ auxin gradient in the pedicel. During anthesis and fruit development stages, the GUS activity across pedicel AZ was lower at anthesis stage than at 2 days before anthesis and 5 days after pollination stages, and abscission assay showed that pedicel at anthesi

Technical Abstract: Auxin plays a critical role in organ abscission. However, the dynamics of auxin signaling gradient during abscission process has not been investigated. Here, we employed a DR5:GUS auxin reporter system to examine temporal and spatial distribution of auxin signaling gradient in response to developmental and environmental cues during pedicel abscission in tomato. Our results showed that in tomato pedicel, GUS activity was predominantly detected in the vascular tissues and higher on the distal side than the proximal side of abscission zone (AZ), suggesting the ‘distal-to-proximal’ auxin gradient in the pedicel. During anthesis and fruit development stages, the GUS activity across pedicel AZ was lower at anthesis stage than at 2 days before anthesis and 5 days after pollination stages, and abscission assay showed that pedicel at anthesis is more prone to abscise than pedicel at 2 days before anthesis and 5 days post pollination stages. Auxin depletion by flower removal or auxin transport inhibitor N-1-napthylphthalamic acid (NPA) treatment reduced auxin gradient across the abscission zones and promoted the abscission. In addition, the auxin signaling gradients were dramatically reduced when plants were exposed to higher temperature and dark condition, resulting in accelerated pedicel abscission. These results suggest that an appropriate auxin response gradient across the pedicel is crucial for initiation of abscission in tomato.