**Genome-Wide Analysis and Cloning of the Apple Stress-Associated Protein Gene Family Reveals** *MdSAP15***, Which Confers Tolerance to Drought and Osmotic Stresses in Transgenic** *Arabidopsis*

#### **Qinglong Dong † , Dingyue Duan † , Shuang Zhao, Bingyao Xu, Jiawei Luo, Qian Wang, Dong Huang, Changhai Liu, Chao Li, Xiaoqing Gong, Ke Mao \* and Fengwang Ma \* ID**

State Key Laboratory of Crop Stress Biology for Arid Areas/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A & F University, Yangling 712100, China; dong19850412@163.com (Q.D.); duandingyue207@foxmail.com (D.D.); zhsh812972738@126.com (S.Z.); 18392610250@163.com (B.X.); m18391488428@163.com (J.L.); wangqian123@nwafu.edu.cn (Q.W.); Mrhaodee@126.com (D.H.); chliu@nwafu.edu.cn (C.L.); lc453@163.com (C.L.); gongxq0103@nwsuaf.edu.cn (X.G.)

**\*** Correspondence: maoke2002@nwsuaf.edu.cn (K.M.); fwm64@nwsuaf.edu.cn or fwm64@sina.com (F.M.); Tel.: +86-029-8708-2613 (K.M.); +86-029-8708-2648 (F.M.)

† These two authors contributed equally to this work.

Received: 8 July 2018; Accepted: 13 August 2018; Published: 21 August 2018

**Abstract:** Stress-associated proteins (SAPs) are novel A20/AN1 zinc finger domain-containing proteins that are now favorable targets to improve abiotic stress tolerance in plants. However, the SAP gene family and their biological functions have not been identified in the important fruit crop apple (*Malus* × *domestica* Borkh.). We conducted a genome-wide analysis and cloning of this gene family in apple and determined that the overexpression of *MdSAP15* enhances drought tolerance in *Arabidopsis* plants. We identified 30 SAP genes in the apple genome. Phylogenetic analysis revealed two major groups within that family. Results from sequence alignments and analyses of 3D structures, phylogenetics, genomics structure, and conserved domains indicated that apple SAPs are highly and structurally conserved. Comprehensive qRT-PCR analysis found various expression patterns for *MdSAPs* in different tissues and in response to a water deficit. A transgenic analysis showed that the overexpression of *MdSAP15* in transgenic *Arabidopsis* plants markedly enhanced their tolerance to osmotic and drought stresses. Our results demonstrate that the SAP genes are highly conserved in plant species, and that *MdSAP15* can be used as a target gene in genetic engineering approaches to improve drought tolerance.

**Keywords:** apple; SAP gene family; expression analysis; function analysis; drought stress; osmotic stress
