Tomato Ovary-to-Fruit Transition is Characterized by a Spatial Shift of mRNAs for Cell Wall Invertase and its Inhibitor with the Encoded Proteins Localized to Sieve Elements

Abstract

Central to understanding fruit development is to elucidate the processes mediating a successful transition from pre-pollination ovaries to newly set fruit, a key step in establishing fruit yield potential. In tomato, cell wall invertase (CWIN) LIN5 and its inhibitor INH1 are essential for fruit growth. However, the molecular and cellular basis by which they exert their roles in ovary-to-fruit transition remains unknown. To address this issue, we conducted a study focusing on ovaries and fruitlets at 2 days before and 2 days after anthesis, respectively. In situ hybridization analyses revealed that LIN5 and INH1 exhibited a dispersed expression in ovaries compared with their phloem-specific expression in fruitlets. Remarkably, LIN5 and INH1 proteins were immunologically co-localized to cell walls of sieve elements (SEs) in ovaries immediately prior to anthesis and in young fruitlets, but were undetectable in provascular bundles of younger ovaries. A burst in CWIN activity occurred during ovary-to-fruit transition. Interestingly, the ovaries, but not the fruitlets, exhibited high expression of a defective invertase, SldeCWIN1, an ortholog of which is known to enhance inhibition of INH on CWIN activity in tobacco. Imaging of a fluorescent symplasmic tracer indicated an apoplasmic phloem unloading pathway operated in ovaries, contrary to the previously observed symplasmic unloading pathway in fruit pericarp. These new data indicate that (1) a phloem-specific patterning of the CWIN and INH mRNAs is induced during ovary-to-fruit transition, and (2) LIN5 protein functions specifically in walls of SEs and increases its activity during ovary-to-fruit transition, probably to facilitate phloem unloading and to generate a glucose signal positively regulating cell division, hence fruit set.

Cell Wall Invertase Promotes Fruit Set under Heat Stress by Suppressing ROS-Independent Cell Death

“…Measurement of enzyme activities in ovaries at 2 d before pollination (dbp) and fruits at 2 dap, the key stages determining fruit set and yield potential (Palmer et al, 2015), revealed there was a 35% to 41% increase of CWIN activity in the transgenic 2-dbp ovaries and 2-dap fruits under both control and LMHS conditions compared with that from wild-type plants (Fig. 3A).…”

“…In tomato, for example, cultivars with higher CWIN activity in anther and fruit had a lower fruit abortion rate under heat stress compared to cultivars with lower CWIN activity Li et al, 2012), and an increase in CWIN activity was observed during ovaryto-fruit transition (Palmer et al, 2015). However, it remains to be seen whether genetically increasing CWIN activity can indeed improve fruit and seed set under heat stress and, if so, what is the underlying physiological and molecular basis.…”

Critical Roles of Vacuolar Invertase in Floral Organ Development and Male and Female Fertilities Are Revealed through Characterization of GhVIN1-RNAi Cotton Plants

“…9). Pertinently, VIN is the major enzyme hydrolyzing Suc in tomato pericarp at the cell division stage (Beauvoit et al, 2014), when unloading occurs symplasmically (Palmer et al, 2015).…”

Sugar Metabolism and Fruit Development in the Tomato

“…Cell wall invertase does not show localization in tomato ovaries before flowering, but interestingly does localize in the fruit vascular tissues at fruit set to transduce the glucose signal by supporting sugar unloading to the fruit, promoting cell division and the resultant fruit set (Palmer et al, 2015). Therefore, the vascular tissue-specific expression of the V-PPase gene may be related to this mechanism involving cell wall invertase because V-PPase may play a role in sugar accumulation, as described above.…”