Transcriptome and translatome changes in germinated pollen under heat stress uncover roles of transporter genes involved in pollen tube growth

Abstract

Plant reproduction is one key biological process that is very sensitive to heat stress and, as a result, enhanced global warming becomes a serious threat to agriculture. In this work, we have studied the effects of heat on germinated pollen of Arabidopsis thaliana both at the transcriptional and translational level. We have used a high‐resolution ribosome profiling technology to provide a comprehensive study of the transcriptome and the translatome of germinated pollen at permissive and restrictive temperatures. We have found significant down‐regulation of key membrane transporters required for pollen tube growth by heat, thus uncovering heat‐sensitive targets. A subset of the heat‐repressed transporters showed coordinated up‐regulation with canonical heat‐shock genes at permissive conditions. We also found specific regulations at the translational level and we have uncovered the presence of ribosomes on sequences annotated as non‐coding. Our results demonstrate that heat impacts mostly on membrane transporters thus explaining the deleterious effects of heat stress on pollen growth. The specific regulations at the translational level and the presence of ribosomes on non‐coding RNAs highlights novel regulatory aspects on plant fertilization.

Heat stress response mechanisms in pollen development

“…Research review New Phytologist (Matsuura et al, 2010;Poidevin et al, 2020). For example, in vitro germinated Arabidopsis pollen responded to severe stress conditions by upregulating heat shock genes in a similar manner to vegetative tissues.…”

Scaling plant responses to high temperature from cell to ecosystem

“…Heat stress imposed during the pollen tetrad and binucleate stages resulted in profound damage to pollen despite elevated levels of sugars, thereby suggesting mechanisms beyond carbohydrate supply as the reason for pollen sterility (Masoomi‐Aladizgeh et al, 2021). Further, heat stress during pollen tube growth in Arabidopsis revealed significant down‐regulation of membrane transporters (Poidevin, Forment, Unal, & Ferrando, 2021). In addition to membrane transporters, the presence of ribosomes on non‐coding RNAs is a novel regulatory aspect of plant fertilization, which indicates the role of alternative players in pollen development and tube growth, apart from sugars (Masoomi‐Aladizgeh et al, 2021; Poidevin et al, 2021).…”

“…Further, heat stress during pollen tube growth in Arabidopsis revealed significant down‐regulation of membrane transporters (Poidevin, Forment, Unal, & Ferrando, 2021). In addition to membrane transporters, the presence of ribosomes on non‐coding RNAs is a novel regulatory aspect of plant fertilization, which indicates the role of alternative players in pollen development and tube growth, apart from sugars (Masoomi‐Aladizgeh et al, 2021; Poidevin et al, 2021).…”

Preferential Ribosome Loading on the Stress-Upregulated mRNA Pool Shapes the Selective Translation under Stress Conditions

“…Recent years have also seen a substantial interest in dissecting the relationship between transcriptional and translational regulations in yeasts, plants and mammals under diverse stresses or across different tissues [15][16][17][18][19][20][21][22][23][24]. However, most of these studies assess the mRNA translation through polysome profiling, which cannot measure the exact number of ribosomes loading on polysome-associated mRNAs for each gene [19][20][21][22][23].…”

“…However, most of these studies assess the mRNA translation through polysome profiling, which cannot measure the exact number of ribosomes loading on polysome-associated mRNAs for each gene [19][20][21][22][23]. By contrast, a few studies comprehensively investigated the translatome based on ribosome footprints [15][16][17][18]24]. For instance, one study in yeast observed that under severe stress conditions such as amino acid depletion or osmotic shock, changes in the transcriptome (mRNAs) correlated well with those in translatome (RPFs), while hardly any or relatively poor correlations were found between these two levels in response to mild stresses induced by calcofluor-white and menadione [15].…”