Comparative Transcriptome Analysis of Arabidopsis Seedlings Under Heat Stress on Whole Plants, Shoots, and Roots Reveals New HS-Regulated Genes, Organ-Specific Responses, and Shoots-Roots Communication.

High temperatures can severely affect plant development and cause a notable decrease in crop yields. Currently, most studies use whole plants that are exposed to steady, high temperatures. This does not reflect the conditions encountered in natural fields, and it overlooks possible differences and coordination between the shoots and roots under heat stress (HS). Here, we analyzed the transcriptome changes in whole plants, shoots, and roots exposed separately to HS. In total, 3346 differentially expressed genes (DEGs) were obtained. Plants in which only the shoots were HS-treated showed minor transcriptional changes compared with whole plants exposed to HS. 62 genes were specifically expressed in HS treatment on shoots, and most of these genes have not been reported to function in HS. We found NAC1 may enhance plant heat tolerance. Utilizing Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analyses, HS-treated shoots showed enhanced gene transcription, protein folding, and MAPK signaling but decreased auxin signaling, while HS-treated roots showed an increase in oxidative stress and suppression of starch and sucrose metabolism. The binding of cis-regulatory elements by transcription factors that act downstream in reactive oxygen species (ROS), abscisic acid (ABA), and brassinosteroid (BR) signaling was significantly enriched at the putative promoters of co-expressed genes in shoots and roots under HS treatments on aboveground tissues or roots. Moreover, 194 core HS-responsive genes were identified from all HS treatments, of which 125 have not been reported to function in HS responses. Among them, we found that REV1 and MYC67 may positively regulate the response of plants to heat shock. This work uncovers many new HS-responsive genes and distinct response strategies employed by shoots and roots following HS exposure. Additionally, ROS, ABA, and BR or their downstream signaling factors may be important components for transmitting heat shock signals between shoots and roots.