Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants

Abstract

High-temperature stress causes abortive male reproductive development in many plant species. Here, we report a putative mechanism of high-temperature injury during anther early development in barley plants (Hordeum vulgare L). Under high-temperature conditions (30 degrees C day/25 degrees C night), cell-proliferation arrest, increased vacuolization, over-development of chloroplasts, and certain abnormalities of the mitochondria, nuclear membrane, and rough endoplasmic reticulum (RER) were observed in developing anther cells, but not in developing ovule cells. Moreover, premature degradation of tapetum cells and premature progression to meiotic prophase in pollen mother cells (PMCs) were also observed. To monitor transcriptional alterations during high-temperature injury, we performed DNA microarray analysis using the 22K Barley1 GeneChip. Expression profiles were captured at four time points during the early development of panicles, and during vegetative growth of seedlings as a control, with or without high-temperature treatment. Abiotic or biotic stress related genes were equally or more dominantly up-regulated in the seedlings exposed to high temperatures compared with the panicles. In contrast, certain genes associated with histones, DNA replication initiation, mitochondria, and ribosomes were specifically repressed in the exposed panicles. In situ hybridization studies indicated that repression locally occurred on the developing anther cells exposed to high temperatures. Microarray analysis also indicated that a series of genes, including a meiosis-specific gene Asy1 and anther-specific lipid transfer protein genes, was prematurely up-regulated at an earlier stage under high-temperature conditions. Real-time quantitative RT-PCR analyses well confirmed the expression differences of certain key genes predicted by the DNA microarrays. These results suggest that high-temperature causes premature progression of anther early development program and fate, such as progression to meiosis of PMCs, cell-proliferation arrest and degradation in anther wall cells, accompanied by comprehensive alterations in transcription.

Auxins reverse plant male sterility caused by high temperatures

“…Our previous result also shows that HT induces expression of auxin response genes in barley seedlings but not in panicles (5). In addition, Figs.…”

“…1 B and D). This stage of development is just before development of tapetum, middle layer, and endothecial cells from the parietal cells (4,5). In plants exposed to HT for <3 days, no morphological abnormalities were observed, and after a temperature downshift, male fertility was recovered (3,4).…”

“…As described, HT treatment was started at the five-leaf stage (2-mm-long panicle), when the tip of the fifth leaf had emerged. Plants were grown at 30°C during the day and 25°C at night for 5 days (3)(4)(5). During this period, pollen mother and tapetum cells developed from anther sporogenous and parietal cells, respectively (4,5).…”

“…Lobell and Field (2) have reported that, at least in the cases of wheat, maize, and barley, there is clearly a negative correlation between worldwide crop yields and increased temperatures, and for these crops, recent warming has resulted in an annual combined loss of ≈40 megatons or $5 billion. Previously, we used double-rowed barley to show that increasing temperatures principally influence the early phase of anther development, causing premature progression through meiosis of pollen mother cells and proliferation arrest and premature degradation of anther wall cells (3)(4)(5). Complete male sterility can result from elevated temperatures for 4 days or longer when they occur during the early phase of anther development, because pollen grains abort (3,4).…”

“…Complete male sterility can result from elevated temperatures for 4 days or longer when they occur during the early phase of anther development, because pollen grains abort (3,4). Several morphological abnormalities can arise during HT injury, including mitochondrial swelling and vacuolization, and comprehensive alterations to transcription in anther wall cells (5). Male sterility caused by abortion of pollen development can be observed widely among other temperature-stressed plant species, such as wheat, tomato, cowpea, and Arabidopsis (6-10).…”