Jong, E. | Search bioRxiv

bioRxiv2024

Enhanced pollen tube performance at high temperature contributes to thermotolerant fruit production in tomato.

Rising temperature extremes during critical reproductive periods threaten the yield of major grain and fruit crops. Flowering plant reproduction depends on development of sufficient numbers of pollen grains and on their ability to generate a cellular extension, the pollen tube, which elongates through the pistil to deliver sperm cells to female gametes for double fertilization. These critical phases of the life cycle are sensitive to temperature and limit productivity under high temperature (HT). Previous studies have investigated the effects of HT on pollen development, but little is known about how HT applied during the pollen tube growth phase affects fertility. Here, we used tomato as a model fruit crop to determine how HT affects the pollen tube growth phase, taking advantage of cultivars noted for fruit production in exceptionally hot growing seasons. We found that exposure to HT solely during the pollen tube growth phase limits fruit biomass and seed set more significantly in thermosensitive cultivars than in thermotolerant cultivars. Importantly, we found that pollen tubes from the thermotolerant Tamaulipas cultivar have enhanced growth in vivo and in vitro under HT. Analysis of the pollen tube transcriptomes response to HT allowed us to develop hypotheses for the molecular basis of cellular thermotolerance in the pollen tube and we define two response modes (enhanced induction of stress responses, and higher basal levels of growth pathways repressed by heat stress) associated with reproductive thermotolerance. Importantly, we define key components of the pollen tube stress response identifying enhanced ROS homeostasis and pollen tube callose synthesis and deposition as important components of reproductive thermotolerance in Tamaulipas. Our work identifies the pollen tube growth phase as a viable target to enhance reproductive thermotolerance and delineates key pathways that are altered in crop varieties capable of fruiting under HT conditions. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=95 SRC="FIGDIR/small/606234v1_ufig1.gif" ALT="Figure 1"> View larger version (35K): org.highwire.dtl.DTLVardef@25e5acorg.highwire.dtl.DTLVardef@98fb1org.highwire.dtl.DTLVardef@1b8b9cborg.highwire.dtl.DTLVardef@adcca4_HPS_FORMAT_FIGEXP M_FIG C_FIG

plant biology↗

bioRxiv2020

AtPIG-S, a predicted Glycosylphosphatidylinositol Transamidase Subunit, is critical for pollen tube growth in Arabidopsis

BackgroundGlycosylphosphatidylinositol (GPI) addition is one of the several post-translational modifications to proteins that increase their affinity for membranes. In eukaryotes, the GPI transamidase complex (GPI-T) catalyzes the attachment of pre-assembled GPI anchors to GPI-anchored proteins (GAPs) through a transamidation reaction. A mutation in AtGPI8 (gpi8-2), the putative catalytic subunit of GPI-T in Arabidopsis, is transmitted normally through the female gametophyte (FG), indicating the FG tolerates loss of GPI transamidation. In contrast, gpi8-2 almost completely abolishes male gametophyte (MG) function. Still, the unexpected finding that gpi8-2 FGs function normally requires further investigation. Additionally, specific developmental defects in the MG caused by loss of GPI transamidation remain poorly characterized. ResultsHere we investigated the effect of loss of AtPIG-S, another GPI-T subunit, in both gametophytes. Like gpi8-2, we showed that a mutation in AtPIG-S (pigs-1) disrupted synergid localization of LORELEI (LRE), a putative GAP critical for pollen tube reception by the FG, yet is transmitted normally through the FG. Conversely, pigs-1 severely impaired male gametophyte (MG) function during pollen tube emergence and growth in the pistil. A pPIGS:PIGS-GFP transgene complemented these MG defects and enabled generation of pigs-1/pigs-1 seedlings, but seemingly failed to rescue the function of AtPIG-S in the sporophyte, as pigs-1/pigs-1, pPIGS:PIGS-GFP seedlings died soon after germination. ConclusionsCharacterization of pigs-1 provided further evidence that the FG tolerates loss of GPI transamidation more than the MG and that the MG compared to the FG may be a better haploid system to study the role of GPI-anchoring. pigs-1 pollen develops normally and thus represent a tool in which GPI anchor biosynthesis and transamidation of GAPs have been uncoupled, offering a potential way to study free GPI in plant development. While previously reported male fertility defects of GPI biosynthesis mutants could have been due either to loss of GPI or GAPs lacking the GPI anchor, our results clarified that the loss of mature GAPs underlie male fertility defects of GPI-deficient pollen grains, as pigs-1 is defective only in the downstream transamidation step. Our study also provided further evidence that GPI transamidation is essential in seedling development.

plant biology↗