Elongation of stigmatic papillae induced by heat stress is associated with disturbance of pollen attachment inArabidopsis thaliana

Abstract

Heat stress can seriously impact on yield production and quality of crops. Many studies 31 uncovered the molecular mechanisms that regulate heat stress responses in plants. 32 Nevertheless, effects of heat stress on the morphology of plants were still not extensively 33 studied. In this study, we observed the detailed morphological changes of reproductive 34 organs in Arabidopsis thaliana caused by heat stress. Larger area of stigma, and shorter 35 length of anthers, filaments and petals were observed in plants subjected to heat stress 36 compared to those under controlled conditions. Scanning electron microscopy (SEM) 37 observation showed that length of stigmatic papillae without pollens seemed to be longer 38 than that with pollens. In addition, classification of stigmas based on pollen attachment 39 patterns together with artificial pollination assay revealed that pollen attachment onto 40 stigma was clearly decreased by heat stress, and indicated that heat induced elongation of 41 stigmatic papillae might be associated with disturbance of pollen attachment onto stigma. 42 Furthermore, histochemical staining experiments revealed that crosstalk between Ca 2+ 43 and NO derived from pollens and O2derived from stigma might be associated with 44 morphological alteration of stigma. 45 46 KEYWORD 47 Heat stress, morphology, SEM, pollen, stigmatic papillae 48 49 50 51 52 53 54 55 56 57 58 59 60 61 Negative effects of abiotic stresses on development of reproductive organs have 62 been reported in recent studies. For instance, drought resulted in abnormal anther 63 development, lower pollen viability, reduced filament elongation, ovule abortion and 64 failure of flowering in Arabidopsis (Su et al., 2013). In contrast, enhanced elongation of 65 stigmatic papillae was observed under high humidity (Takeda et al., 2018). These studies 66 indicated that water status in surrounding environments alter the developmental patterns 67 of reproductive organs, leading to decrease in seed production. Heat stress was also shown 68 to negatively affect seed production (Katano et al., 2018b; Suzuki et al., 2013; Tunc-69 Ozdemir et al., 2013). We can therefore expect that decrease in seed production caused 70 by heat stress might be at least partially attributed to morphological alterations in 71 reproductive organs. Indeed, it has been well known that heat stress dramatically impacts 72 on development of anthers and pollens (Katano et al., 2018a; Rieu and Twell, 2017). 73 However, effects of heat stress on development of other reproductive organs are still 74 largely unknown. In addition, only few studies focused on detailed morphological 75 alterations of reproductive organs caused by heat stress, despite the remarkable progress 76 of researches uncovering molecular mechanisms that regulate response in reproductive 77 organs to heat stress.78In this study, to dissect the morphological alteration of reproductive organs induced 79 by heat stress, we investigated the size of each reproductive organ in Arabidopsis plants 80 gro...

The neglected other half ‐ role of the pistil in plant heat stress responses

“…Both pollination and fertilization processes are extremely sensitive to heat stress. For instance, heat stress decreased the number of pollen grains that adhered to the stigmatic surface affecting pollen receptivity in different plant species (Arabidopsis [ Arabidopsis thaliana ], 40/21°C, Katano et al, 2019; chickpea, 40/30°C and 45/35°C, Kumar et al, 2013; peach [ Amygdalus persica L.], 30°C, Carpenedo et al, 2020; wheat, 35/25°C, Prasad & Djanaguiraman, 2014). In canola, increased temperature shortened the stigma nectar secretion period, which contributed to a gradual decrease in effectiveness of the pollinator‐based pollination (Chabert et al, 2018).…”

“…Studies are referenced according to the crop, with numbers in parenthesis in the legend aligned with the number and related change listed above in the grey box. Crops and related references: tomato—[1] (Pan et al, 2017); [8] (Mareri et al, 2016); [9] (Liu, Offler, & Ruan, 2016); rice—[2] (Wu et al, 2019); [13] (Jiang et al, 2020); [14] ( Zhang, Li, Chen, et al, 2018); chickpea—[3] (Kumar et al, 2013); wheat—[4] (Prasad & Djanaguiraman, 2014); arabidopsis—[5] (Katano, Oi, & Suzuki, 2019); peach—[6] (Carpenedo, Bassols, Franzon, Byrne, & Silva, 2020); canola—[7] (Chabert, Lemoine, Cagnato, Morison, & Vaissière, 2018); cotton—[10] (Loka & Oosterhuis, 2016); [11] (Snider, Oosterhuis, Skulman, & Kawakami, 2009); [12] (Snider, Oosterhuis, Loka, & Kawakami, 2011a); pea—[15] (Savada, Ozga, Jayasinghege, Waduthanthri, & Reinecke, 2017); pearl millet—[16] (Djanaguiraman, Perumal, Ciampitti, et al, 2018). AGP, Arabinogalactan Proteins; ROS, Reactive Oxygen Species [Colour figure can be viewed at wileyonlinelibrary.com]…”

Failure of Pollen Attachment to the Stigma Triggers Elongation of Stigmatic Papillae in Arabidopsis thaliana

“…This work was supported by Sophia University. This manuscript has been released as a pre-print at bioRxiv, (Katano et al, 2019) (https://www.biorxiv.org/content/ 10.1101/2019.12.21.885640v1.abstract).…”

“…This work was supported by Sophia University. This manuscript has been released as a pre-print at bioRxiv, ( Katano et al, 2019 ) ( ).…”