Cold stress induces malformed tomato fruits by breaking the feedback loops of stem cell regulation in floral meristem

Abstract

Summary Fruit malformation is a major constrain in fruit production worldwide resulting in substantial economic losses. The farmers for decades noticed that the chilling temperature before blooming often caused malformed fruits. However, the molecular mechanism underlying this phenomenon is unclear. Here we examined the fruit development in response to cold stress in tomato, and demonstrated that short‐term cold stress increased the callose accumulation in both shoot apical and floral meristems, resulting in the symplastic isolation and altered intercellular movement of WUS. In contrast to the rapidly restored SlWUS transcription during the recovery from cold stress, the callose removal was delayed due to obstructed plasmodesmata. The delayed reinstatement of cell‐to‐cell transport of SlWUS prevented the activation of SlCLV3 and TAG1, causing the interrupted feedback inhibition of SlWUS expression, leading to the expanded stem cell population and malformed fruits. We further showed that the callose dynamics in response to short‐term cold stress presumably exploits the mechanism of bud dormancy during the seasonal growth, involving two antagonistic hormones, abscisic acid and gibberellin. Our results provide a novel insight into the cold stress regulated malformation of fruit.

The FW2.2/CNR protein regulates cell-to-cell communication in tomato by modulating callose deposition at plasmodesmata

“…As reviewed by Han et al (2014b), TFs are well characterized examples of such signalling molecules that could play an important part in the determination of fruit size. Recently, it was shown that a cold stress increases callose accumulation in the FM of tomato plants, resulting in impaired feedback loops which regulate the activity of WUSCHEL (WUS) (Wu et al, 2023). The TF WUS specifies the maintenance of stem cell activity in FM, and therefore a deregulation of WUS activity impacts the number of carpel primordia, and ultimately the number of locules inside the fruit.…”

“…The discovery of the FW2. feedback loops which regulate the activity of WUSCHEL (WUS) (Wu et al, 2023).…”

“…As a consequence of cold stress, CalS genes are induced and promote the callose deposition in the FM, which blocks the PDmediated symplastic connection and alters the cell-to-cell movement of WUS which no longer can exert its negative regulatory action on CLAVATA3 and AGAMOUS. As a result, the activity of WUS is not terminated in due time, which leads to increased cell divisions in the FM producing extra carpels and locules during fruit organogenesis (Wu et al, 2023). Interestingly, we observed similar trends in our transgenics plants: a higher number of locules resulting from increased cell divisions in FM in loss-of-function CR-fw2.2 lines, as callose deposition was increased, and the opposite effects in gain-of-function 35::FW2.2 lines (Figure 5C).…”

Characterization and expression profiles of WUSCHEL-related homeobox (WOX) gene family in cultivated alfalfa (Medicago sativa L.)

“…Previous reports mainly focused on WOX regulation of plant development and growth, but few studies investigated the roles of WOXs in diverse stresses. Tomato SlWUS and Arabidopsis AtWOX6 are involved in cold stress through CBF-independent pathways [ 42 , 59 ]. Rice OsWOX11 and OsWOX13 have been reported to be involved in drought resistance [ 36 , 44 ].…”

APP1/NTL9‐CalS8 module ensures proper phloem differentiation by stabilizing callose accumulation and symplastic communication

“…In plants, intercellular communication and molecular exchanges occur through apoplastic and symplastic pathways. Symplastic communication coordinates diverse signals during biological processes, including plant growth, development, and environmental responses (Faulkner, 2018; Gaudioso‐Pedraza et al ., 2018; Azim & Burch‐Smith, 2020; Mellor et al ., 2020; Li et al ., 2022; Wu et al ., 2023). Plasmodesmata provide a direct symplastic channel for cell‐to‐cell molecular transport and play roles in phloem development and root growth (Benitez‐Alfonso, 2014; Yadav et al ., 2014; Sevilem et al ., 2015; Lee & Frank, 2018).…”