Effects of different temperature regimes on flower development, microsporogenesis and fertility in bolting garlic (Allium sativum)

Abstract

Garlic (Allium sativum L.) cultivars do not develop fertile flowers and seeds. Therefore, garlic production and improvement depend exclusively on vegetative propagation. Recent advances in garlic research have enabled fertility restoration and the discovery of fertile and male-sterile genotypes; however, the environmental regulation of the reproductive process is still not clear. Garlic seeds are successfully produced in the Mediterrenean region, where the photoperiod is relatively short, whereas spring and summer temperatures are high. We hypothesise that, in bolting garlic, various stages of florogenesis are differentially regulated by temperature and that high temperatures might obstruct pollen production. The effects of eight combinations of controlled growth temperatures on fertile and male-sterile garlic clones were studied. In both genotypes, a gradual temperature increase before and during anthesis favoured intact flower development. Surprisingly, continuous exposure to moderate temperatures during the entire growth period resulted in poor flowering, anther abortion and reduced pollen production. In the male-sterile genotype, no growth regime improved pollen production, which is controlled by genetic mechanisms. In the male-fertile genotype, gradual temperature increase supported pollen production but a sharp transition to high temperatures resulted in rapid flower senescence and pollen abortion, thus supporting our research hypothesis. In both fertile and male-sterile plants, the most vulnerable phase of microsporogenesis is the unicellular microspore stage. Tapetal malformation is the major cause for malnutrition of the microspores, with consequent production of nonviable pollen grains.

The effect of high temperature stress on male and female reproduction in plants

“…Microscopic confirmation of abortion at this stage following exposure to temperatures ≥30 • C has been reported for cereal and eudicot crops to include rice ( Fig. 3D; Bagha, 2014), wheat (Saini and Aspinall, 1982;Saini et al, 1984), sorghum (Jain et al, 2007), barley (Sakata et al, 2000;Oshino et al, 2007), snap beans (Suzuki et al, 2001), cowpea (Ahmed et al, 1992), tomato (Iwahori, 1965), Brachypodium distachyon (Harsant et al, 2013), cotton (Min et al, 2014), and garlic (Mayer et al, 2015). The uninucleate stage is more sensitive in the low 30 • C range in cool-season crops such as barley, wheat, and garlic whereas temperatures in the mid-to-upper 30 • C range effect development in warm-season crops.…”

Flower orientation influences floral temperature, pollinator visits and plant fitness

“…Ample published literature has described how heat stress negatively affects plant fitness through impaired pollen donation (also referred to as male fitness), including inhibition of pollen development, pollen emergence and fertility (Hedhly, 2011; Giorno et al ., 2013; Paupière et al ., 2014; Mayer et al ., 2015; Dwivedi et al ., 2017; Begcy et al ., 2019; Raja et al ., 2019). Negative effects of heat stress on fitness through fruit and seed production (also referred to as female fitness) have been less well explored, but emerging studies on cereal pistils have shown that the accumulation of reactive oxygen species under high temperatures can reduce stigma receptivity and pollination (Jagadish, 2020).…”

Identification of male-fertility gene AsaNRF1 and molecular marker development in cultivated garlic (Allium sativum L.)

“…Cultivated garlic is a natural male-sterile material and an ideal female parent for hybrid production. Limited by the availability of male-fertile garlic cultivars, research has mainly focused on the analysis of organ-and tissue-specific gene expression in garlic (Allium sativum L.) using transcriptome data (Kamenetsky et al, 2015;Shemesh-Mayer et al, 2015;Havey and Ahn, 2016). The release of the garlic genome (Sun et al, 2020;Hao et al, 2023), and especially the availability of a fertile garlic cultivar G398, which has been identified and maintained by our group for more than 20 years, provide a strong foundation for a systematic analysis of the molecular mechanisms underlying the sterility of garlic cultivars.…”

“…Normal tapetum function requires the properly timed initiation and progression of programmed cell death (PCD) ( Papini et al., 1999 ; Kawanabe et al., 2006 ; Ji et al., 2013 ). Non-regulated PCD of the tapetum can lead to energy deficiency and consequent pollen abortion in garlic (Shemesh- Mayer et al., 2015 ). Abnormal tapetal development has been previously described as a possible cause of male sterility in garlic ( Novak, 1972 ; Shemesh-Mayer et al., 2015 ), onion ( Allium cepa ) ( Holford et al., 1991 ), lily ( Lilium Asiatic ) ( Wang et al., 2019 ) and Arabidopsis thaliana ( Chaudhury et al., 1994 ).…”