Summary The firmness of fleshy fruit crops has a significant effect on their quality, consumer preference, shelf life and transportability. In a combined quantitative trait locus and genome‐wide association studies study of apple fruit texture, we identified a mutation (C‐G) in the ethylene response factor‐associated amphiphilic repression (EAR) motif in the coding region of the apple ETHYLENE RESPONSE FACTOR4 (ERF4) gene. Chromatin immunoprecipitation sequencing showed that ERF4 binds to the promoter of ERF3, which is involved in regulation of ethylene biosynthesis. The EAR mutation in ERF4 results in reduced repression of ERF3 expression, which is turn promotes ethylene production and loss of fruit firmness. ERF4 acts as a transcriptional repressor whose activity is modulated by a TOPLESS co‐repressor 4 (TPL4)‐binding EAR repression motif. Biolayer interferometry analysis showed that the mutation in the EAR motif causes a reduction in the interaction with TPL4. Suppression of ERF4 or TPL4 promoted fruit ripening and ethylene production. Taken together, our results provide insights into how ERF4 allelic variation underlies an important fruit quality trait.

SummaryIron (Fe) is an essential plant nutrient and its deficiency typically limits plant growth. Long non‐coding (lnc) RNAs are involved in adaptive responses to nutrient stress; however, it is not known whether they function in the regulation of the canonical Fe‐deficiency response. The expression of Malus domestica (apple) lncRNA MSTRG.85814 is induced by Fe deficiency, as identified by high‐throughput strand‐specific RNA‐seq analysis of an apple homograft system. MSTRG.85814 has a complex structure, with 13 predicted RNA sequence variants, four of which are upregulated in the roots of plants experiencing Fe deficiency. We found that one MSTRG.85814 splice variant (MSTRG.85814.11) positively modulated its cis target mRNA derived from the small auxin upregulated gene SAUR32. This in turn promoted the expression of SAUR32 and caused an increase in the expression of a plasma membrane proton ATPase, AHA10. Using a pH imaging technique, a significant decrease in the apoplastic pH was observed to occur in the root tips of MSTRG.85814.11 or SAUR32‐overexpressing apple plants. Thus MSTRG.85814.11 was shown to positively promote SAUR32 expression, which then activated proton extrusion involved in the Fe‐deficiency response. These results reveal a mechanism by which lncRNA promotes environmental Fe‐deficiency stress adaption.

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Plant AT-rich sequences and zinc-binding proteins (PLATZ) play crucial roles in response to environmental stresses. Nevertheless, PLATZ gene family has not been systemically studied in Rosaceae species, such as in apple, pear, peach, or strawberry. In this study, a total of 134 PLATZ proteins were identified from nine Rosaceae genomes and were classified into seven phylogenetic groups. Subsequently, the chromosomal localization, duplication, and collinearity relationship for apple PLATZ genes were investigated, and segmental duplication is a major driving-force in the expansion of PLATZ in Malus. Expression profiles analysis showed that PLATZs had distinct expression patterns in different tissues, and multiple genes were significantly changed after drought and ABA treatments. Furthermore, the co-expression network combined with RNA-seq data showed that PLATZ might be involved in drought stress by regulating ABA signaling pathway. In summary, this study is the first in-depth and systematic identification of PLATZ gene family in Rosaceae species, especially for apple, and provided specific PLATZ gene resource for further functional research in response to abiotic stress.

Long-distance mobile mRNAs play key roles in gene regulatory networks that control plant development and stress tolerance. However, the mechanisms underlying species-specific delivery of mRNA still need to be elucidated. Here, the use of grafts involving highly heterozygous apple (Malus) genotypes allowed us to demonstrate that apple (Malus domestica) oligopeptide transporter3 (MdOPT3) mRNA can be transported over a long distance, from the leaf to the root, to regulate Fe uptake; however, the mRNA of Arabidopsis (Arabidopsis thaliana) oligopeptide transporter 3 (AtOPT3), the MdOPT3 homolog from A. thaliana, does not move from shoot to root. Reciprocal heterologous expression of the two types of mRNAs showed that the immobile AtOPT3 became mobile and moved from the shoot to the root in two woody species, Malus and Populus, while the mobile MdOPT3 became immobile in two herbaceous species, A. thaliana and tomato (Solanum lycopersicum). Furthermore, we demonstrated that the different transmissibility of OPT3 in A. thaliana and Malus might be caused by divergence in RNA-binding proteins (RBPs) between herbaceous and woody plants. This study provides insights into mechanisms underlying differences in mRNA mobility and validates the important physiological functions associated with this process.

Iron (Fe) plays an important role in cellular respiration and catalytic reactions of metalloproteins in plants and animals. Plants maintain iron homeostasis through absorption, translocation, storage, and compartmentalization of iron via a cooperative regulative network. Here, we showed different physiological characteristics in the leaves and roots of Malus baccata under Fe sufficiency and Fe deficiency conditions and propose that MbHY5 (elongated hypocotyl 5), an important transcription factor for its function in photomorphogenesis, participated in Fe deficiency response in both the leaves and roots of M. baccata. The gene co-expression network showed that MbHY5 was involved in the regulation of chlorophyll synthesis and Fe transport pathway under Fe-limiting conditions. Specifically, we found that Fe deficiency induced the expression of MbYSL7 in root, which was positively regulated by MbHY5. Overexpressing or silencing MbYSL7 influenced the expression of MbHY5 in M. baccata.

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