The genus of Actinidia consists of the popular kiwifruits consuming worldwide. Most kiwifruit species are naturally distributed in warm and moist environments. So, they are vulnerable to high levels of heat stress. Till now, genetic basis of kiwifruit thermotolerance has remained largely unexplored. Here, we uncover a natural variation responsible for thermotolerance in kiwifruit species. We reveal that thermotolerant kiwifruit species have increased expression of AcEGY3, a gene encoding a chloroplast-localized protein, which can promote expression of nuclear thermotolerance genes via H₂O₂-dependent retrograde signaling. We show that natural variation in the promoter of AcEGY3 constitute a binding site for the heat stress-inducible transcription factor AcGATA1. The increased expression of AcEGY3 is regulated by AcGATA1 and its possible interaction with another transcription factor AcHSFA2-2. This natural variation is absent from the thermosensitive kiwifruit species. Collectively, our results reveal genetic basis of kiwifruit thermotolerance and set the foundation for breeding thermotolerant kiwifruits cultivars.

Kiwifruit (Actinidia chinensis) is commonly covered by fruit hairs (trichomes) that affect kiwifruit popularity in the commercial market. However, it remains largely unknown which gene mediates trichome development in kiwifruit. In this study, we analyzed two kiwifruit species, A. eriantha (Ae) with long, straight, and bushy trichomes and A. latifolia (Al) with short, distorted, and spare trichomes, by second- and third-generation RNA sequencing. Transcriptomic analysis indicated that the expression of the NAP1 gene, a positive regulator of trichome development, was suppressed in Al compared with that in Ae. Additionally, the alternative splicing of AlNAP1 produced two short transcripts (AlNAP1-AS1 and AlNAP1-AS2) lacking multiple exons, in addition to a full-length transcript of AlNAP1-FL. The defects of trichome development (short and distorted trichome) in Arabidopsis nap1 mutant were rescued by AlNAP1-FL but not by AlNAP1-AS1. AlNAP1-FL gene does not affect trichome density in nap1 mutant. The qRT−PCR analysis indicated that the alternative splicing further reduces the level of functional transcripts. These results indicated that the short and distorted trichomes in Al might be caused by the suppression and alternative splicing of AlNAP1. Together, we revealed that AlNAP1 mediates trichome development and is a good candidate target for genetic modification of trichome length in kiwifruit.