AtHVA22 gene family in Arabidopsis: phylogenetic relationship,ABA and stress regulation,and tissue-specific expression

HVA22 is an ABA- and stress-inducible gene first isolated from barley (Hordeum vulgare L.). Homologues of HVA22 have been found in plants, animals, fungi and protozoa, but not in prokaryotes, suggesting that HVA22 plays a unique role in eukaryotes. Five HVA22 homologues, designated AtHVA22a, b, c, d and e, have been identified in Arabidopsis. These five AtHVA22 homologues can be separated into two subfamilies, with AtHVA22a, b and c grouped in one subfamily and AtHVA22d and e in the other. Phylogenetic analyses show that AtHVA22d and e are closer to barley HVA22 than to AtHVA22a, b and c, suggesting that the two subfamilies had diverged before the divergence of monocots and dicots. The distribution and size of exons of AtHVA22 homologues and barley HVA22 are similar, suggesting that these genes are descendents of a common ancestor. AtHVA22 homologues are differentially regulated by ABA, cold, dehydration and salt stresses. These four treatments enhance AtHVA22a, d and e expression, but have little or even suppressive effect on AtHVA22c expression. ABA and salt stress induce AtHVA22b expression, but cold stress suppresses ABA induction of this gene. Expression of AtHVA22d is the most tightly regulated by these four treatments among the five homologues. In general, AtHVA22 homologues are expressed at a higher level in flower buds and inflorescence stems than in rosette and cauline leaves. The expression level of these homologues in immature siliques is the lowest among all tissues analyzed. It is suggested that some of these AtHVA22 family members may play a role in stress tolerance, and others are involved in plant reproductive development.     

The stress- and abscisic acid-induced barley gene HVA22: developmental regulation and homologues in diverse organisms

Abscisic acid (ABA) induces the expression of a battery of genes in mediating plant responses to environmental stresses. Here we report one of the early ABA-inducible genes in barley (Hordeum vulgare L.), HVA22, which shares little homology with other ABA-responsive genes such as LEA (late embryogenesis-abundant) and RAB (responsive to ABA) genes. In grains, the expression of HVA22 gene appears to be correlated with the dormancy status. The level of HVA22 mRNA increases during grain development, and declines to an undetectable level within 12 h after imbibition of non-dormant grains. In contrast, the HVA22 mRNA level remains high in dormant grains even after five days of imbibition. Treatment of dormant grains with gibberellin (GA) effectively breaks dormancy with a concomitant decline of the level of HVA22 mRNA. The expression of HVA22 appears to be tissue-specific with the level of its mRNA readily detectable in aleurone layers and embryos, yet undetectable in the starchy endosperm. The expression of HVA22 in vegetative tissues can be induced by ABA and environmental stresses, such as cold and drought. Apparent homologues of this barley gene are found in phylogenetically divergent eukaryotic organisms, including cereals, Arabidopsis, Caenorhabitis elegans, man, mouse and yeast, but not in any prokaryotes. Interestingly, similar to barley HVA22, the yeast homologue is also stress-inducible. These observations suggest that the HVA22 and its homologues encode a highly conserved stress-inducible protein which may play an important role in protecting cells from damage under stress conditions in many eukaryotic organisms.     

Cold-induced mRNAs accumulate with different kinetics in barley coleoptiles

The effect of cold treatment on gene expression in two different barley (Hordeum vulgare L.) cultivars has been studied. Cold stress induced a set of new mRNAs as determined by in-vitro translation of coleoptile RNA obtained from control and stressed seedlings. These mRNAs accumulated with different kinetics, and the cold-induced proteins could be grouped into five categories. The first category (a) is represented by a single protein with M_r of 75 kDa that reaches its highest level of expression after 6 h at 5°C. This polypeptide readily accumulates in the plant tissues and it can be detected when proteins separated by two-dimensional electrophoresis are stained with silver nitrate. The other polypeptides appear later during the 1- to 4-d stress period (protein groups b and c), increase (group d), or decrease during the period of treatment (group e). Only minor differences between the two cultivars with different cold-resistance capacities were found when the in-vitro translation products were compared. The results obtained demonstrate that several mRNAs are specifically expressed as a response to cold treatment in barley coleoptiles.Abbreviations 2-D two-dimensional - IEF isoelectrofocusing - M_r relative molecular weight - poly(A) polyadenylated - SDS-PAGE sodium dodecyl sulfate-polyacrylamide gel electrophoresis     

Autophagy Is Enhanced and Floral Development Is Impaired in AtHVA22d RNA Interference Arabidopsis

Autophagy is an intracellular process in which a portion of cytoplasm is transported into vacuoles for recycling. Physiological roles of autophagy in plants include recycling nutrients during senescence, sustaining life during starvation, and the formation of central digestive vacuoles. The regulation of autophagy and the formation of autophagosomes, spherical double membrane structures containing cytoplasm moving toward vacuoles, are poorly understood. HVA22 is a gene originally cloned from barley (Hordeum vulgare), which is highly induced by abscisic acid and environmental stress. Homologs of HVA22 include Yop1 in yeast, TB2/DP1 in human, and AtHVA22a to -e in Arabidopsis (Arabidopsis thaliana). Reverse genetics followed by a cell biology approach were employed to study the function of HVA22 homologs. The AtHVA22d RNA interference (RNAi) Arabidopsis plants produced small siliques with reduced seed yield. This phenotype cosegregated with the RNAi transgene. Causes of the reduced seed yield include short filaments, defective carpels, and dysfunctional pollen grains. Enhanced autophagy was observed in the filament cells. The number of autophagosomes in root tips of RNAi plants was also increased dramatically. The yop1 deletion mutant of Saccharomyces cerevisiae was used to verify our hypothesis that HVA22 homologs are suppressors of autophagy. Autophagy activity of this mutant during nitrogen starvation increased in 5 min and reached a plateau after 2 h, with about 80% of cells showing autophagy, while the wild-type cells exhibited low levels of autophagy following 8 h of nitrogen starvation. We conclude that HVA22 homologs function as suppressors of autophagy in both plants and yeast. Potential mechanisms of this suppression and the roles of abscisic acid-induced HVA22 expression in vegetative and reproductive tissues are discussed.     

Nomenclature of the bacteriochlorophyllsc,d, ande

A system for nomenclature of the various homologues of the bacteriochlorophyllsc(1),d(2), ande(3) is presented.     

Developmental and organ-specific expression of an ABA- and stress-induced protein in barley

An mRNA species, HVA1, has been shown to be rapidly induced by abscisic acid (ABA) in barley aleurone layers (Hong, Uknes and Ho, Plant Mol Biol 11: 495–506, 1988). In the current work we have investigated the expression of HVA1 in other organs of barley plants. In developing seeds, HVA1 mRNA is not detected in starchy endosperm cells, yet it accumulates in aleurone layers and embryo starting 25 days after anthesis, and its level remains high in these organs in dry seeds. Although the levels of HVA1 mRNA are equivalent in the dry embryos of dormant and nondormant barley seeds, upon imbibition HVA1 mRNA declines much slower in the dormant than in the nondormant embryos. The HVA1 mRNA and protein levels are highly induced by ABA treatment in all organs of 3-day-old seedlings. However, the induction in the leaf of 7-day-old seedlings is less than one tenth the level observed in the leaf of 3-day-old seedlings. In the leaf, HVA1 mRNA and protein are induced mainly at the base. These observations indicate that the expression of HVA1 is under developmental regulation. Besides the HVA1 protein, a smaller protein (p20) of approximately 20 kDa cross-reacting with anti-HVA1 polyclonal antibodies, is induced by ABA in barley seedlings but not in seeds. HVA1 mRNA is induced by drought, NaCl, cold or heat treatment. Similar to ABA treatment, the drought induction of HVA1 occurs in all the tissues of 3-day-old seedling, but the induction decreases dramatically in the leaf of 7-day-old plants. The significance of organ-specific, developmentally regulated, and stress-induced expression of HVA1 is discussed.     

Identification of the major chlorosomal bacteriochlorophylls of the green sulfur bacteria Chlorobium vibrioforme and Chlorobium phaeovibrioides; their function in lateral energy transfer

The chlorosomal bacteriochlorophyll (BChl) composition of the green sulfur bacteria Chlorobium vibrioforme and Chlorobium phaeovibrioides was investigated by means of normal-phase high-performance liquid chromatography. From both species a number of homologues was isolated, which were identified by absorption and ²⁵²Cf-plasma desorption mass spectroscopy. Besides BChl d, C. vibrioforme contained a significant amount of BChl c, which may provide an explanation for the previous observation of at least two spectrally different pools of BChl in the chlorosomes of green sulfur bacteria (Otte et al. 1991). C. phaeovibrioides contained various homologues of BChl e only. Absorption spectra in acetone of BChl c, d and e, as well as bacteriopheophytin e are presented. No systematic differences were found for the various homologues of each pigment. In addition to farnesol, the mass spectra revealed the presence of various minor esterifying alcohols in both species, including phytol, oleol, cetol and 4-undecyl-2-furanmethanol, as well as an alcohol of low molecular mass, which is tentatively assumed to be decenol.Abbreviations BChl bacteriochlorophyll - BPh bacteriopheophytin (used as a general name for the Mg-free compound, irrespective of the esterifying alcohol) - HPLC high-performance liquid chromatography     

Overexpression of barley <Emphasis Type="Italic">hva1</Emphasis> gene in creeping bentgrass for improving drought tolerance

The objectives of this study were to test the feasibility of introducing barley hva1 gene, a LEA3 member, into perennial grass species using the Agrobacterium-mediated transformation technique and to determine whether heterologous expression of hva1 would alleviate water-deficit injury in grass species. Creeping bentgrass (Agrostis stolonifera var. palustris), a drought-intolerant grass species, was transformed transiently or stably using three different promoters in conjunction with the downstream report/target genes. Two abscisic acid (ABA)-inducible promoters, ABA1 and ABA2 derived from ABA-response complex (ABRC3) were used to examine stress-responsive expression of the green fluorescent protein (GFP). Transient expression of GFP demonstrated the inducibility of ABA1 and ABA2 promoters in response to exogenous ABA application. The ABA2 promoter was further studied for stress-responsive expression of hva1 and a maize Ubi-1 promoter was tested for constitutive expression of the gene. In the T₀ generation, the Ubi-1::hva1 transformants displayed variable expression levels of HVA1 protein under normal growth conditions. The hva1 gene in the ABA2::hva1 transformants maintained low expression under well-watered conditions, but was upregulated under water-deficit conditions. The tolerance to water deficit of T₀ transgenic lines was assessed by measuring leaf relative water content and visually rating the severity of leaf wilting during to water stress. Under water-stressed conditions, some transgenic lines maintained high water content in leaves and showed significantly less extent of leaf wilting compared with non-transgenic control plants. These results indicated that the introduction of barley hva1 gene using constitutive or stress-inducible promoters lessened water-deficit injury in creeping bentgrass, suggesting that heterologous expression of LEA3 protein genes may enhance the survival ability of creeping bentgrass in water limiting environments.     

A barley (Hordeum vulgare L.) LEA3 protein, HVA1, is abundant in protein storage vacuoles

The HVA1 protein belongs to the LEA3 group, which is expressed during the late stage of seed maturation. It is also induced by exogenous abscisic acid (ABA) and a variety of environmental stresses in germinating barley (Hordeum vulgare L.). In the present work, the potential role of HVA1 was investigated by studying its tissue distribution and subcellular localization in mature and stressed seeds by immuno-microscopic methods. In the mature seed, HVA1 protein was detected in all tissues except the non-living starchy endosperm. During germination the amount of HVA1 protein decreased but did not totally disappear. Incubation with 100 μM ABA, cold treatment or drought stress dramatically increased HVA1 expression in the germinated seed. In this work, the distribution of a LEA3 group protein was studied in a cereal seed for the first time by immuno-electron microscopy. In the scutellum and aleurone layer, HVA1 was localized both in the cytoplasm and protein storage vacuoles (PSVs). HVA1 protein was found to be threefold more abundant in PSVs than in the cytoplasm of an unstressed seed tissue. The ratio increased with ABA or stress treatments to at least ninefold. The role of HVA1 in PSVs remains unclear: a previously suggested possibility is ion sequestration to prevent precipitation during stress. On the other hand, HVA1 protein could also be degraded in PSVs. HVA1 protein does not have the signal peptide typical of proteins which are glycosylated and targeted into the vacuole via the Golgi complex. Because HVA1 is not glycosylated, it may use an alternative, ER-independent vacuolar pathway, also found in yeast cells.     

Cloning of cDNAs for genes that are early-responsive to dehydration stress (ERDs) inArabidopsis thaliana L.: identification of three ERDs as HSP cognate genes

InArabidopsis thaliana L., accumulation of abscisic acid (ABA) began to increase 2 h after plants had been subjected to dehydration stress and reached maximum levels after 10h. Differential hybridization was used to isolate 26Arabidopsis cDNAs with gene expression induced by a 1 h dehydration treatment. The cDNA clones were classified into 16 groups based on Southern blot hybridization, and named ERD (early-responsive todehydration) clones. Partial sequencing of the cDNA clones revealed that three ERDs were identical to those of HSP cognates (Athsp70-1, Athsp81-2, and ubiquitin extension protein). Dehydration stress strongly induced the expression of genes for the three ERDs, while application of ABA, which is known to act as a signal transmitter in dehydration-stressed plants, did not significantly affect the ERD gene expression. This result suggests that these HSP cognates are preferentially responsive to dehydration stress inA. thaliana, and that signaling pathways for the expression of these genes under conditions of dehydration stress are not mainly mediated by ABA. We also discuss the possible functions of these three ERD gene products against dehydration stress.     

Assembly and composition of the chlorophyll a-b light-harvesting complex of barley (Hordeum vulgare L.): Immunochemical analysis of chlorophyll b-less and chlorophyll b-deficient mutants

The chlorina-f2 mutant of barley (Hordeum vulgare L.) contains no chlorophyll b in its light-harvesting antenna, whereas the chlorina-103 mutant contains approximately 10% of the chlorophyll b found in wild-type. The absolute chlorophyll antenna size for Photosystem-II in wild-type, chlorina-103 and chlorina-f2 mutant was 250, 58 and 50 chlorophyll molecules, respectively. The absolute chlorophyll antenna size for Photosystem-I in wild-type, chlorina-103 and chlorina-f2 mutant was 210, 137 and 150 chlorophyll molecules, respoectively. In spite of the smaller PS I antenna size in the chlorina mutants, immunochemical analysis showed the presence of polypeptide components of the LHC-I auxiliary antenna with molecular masses of 25, 19.5 and 19 kDa. The chlorophyll a-b-binding LHC-II auxiliary antenna of PS II contained five polypeptide subunits in wild-type barley, termed a, b, c, d and e, with molecular masses of 30, 28, 27, 24 and 21 kDa, respectively. The polypeptide composition of the LHC-II auxiliary antenna of PS II was found to be identical in the two mutants, with only the 24 kDa subunit d present at an equal copy number per PS II in each of the mutants and in the wild-type barley. This d subunit assembles stably in the thylakoid membrane even in the absence of chlorophyll b and exhibits flexibility in its complement of bound chlorophylls. We suggest that polypeptide subunit d binds most of the chlorophyll associated with the residual PS II antenna in the chlorina mutants and that is proximal to the PS II-core complex.Abbreviations CP chlorophyll-protein - LHC the chlorophyll a-b binding light-harvesting complex - LHC-II subunit a the Lhcb4/5 gene product - subunit b the Lhcb1 gene product - subunit c Lhcb2 the gene product - subunit d the Lhcb3 gene product - subunit e the Lhcb6 gene product - PMSF phenylmethane sulphonyl fluoride - RC reaction center - Q_A the primary quinone electron acceptor of Photosystem-II - P700 the reaction center of PS I     

Coalescent processes and relaxation of selective constraints leading to contrasting genetic diversity at paralogs AtHVA22d and AtHVA22e in Arabidopsis thaliana

Duplicate loci offer a very powerful system for understanding the complicated genome structure and adaptive evolution of a gene family. In this study, the genetic variation at paralogs AtHVA22d and AtHVA22e, members of an ABA- and stress-inducible gene family, is examined in the selfing Arabidopsis thaliana. Population genetic analysis indicates contrasting levels of nucleotide diversity at overall exon sequence and nonsynonymous sites between AtHVA22d (pi = 0.00337, pi(rep) = 0.00158) and AtHVA22e (pi = 0.00054, pi(rep) = 0.00023). The fact of Ka/Ks ratios significantly less than 1 in all sequences indicates that both genes are functional and subjected to purifying selection. In addition, rooted at barley HVA22, accelerated evolution is detected at replacement changes in the AtHVA22d locus, indicating relaxation of purifying selection after gene duplication. However, relative rate tests reveal no deviation from the neutrality at synonymous sites between the two paralogs. Based on clock-like evolution, the rate of synonymous substitution is estimated at 1.83 x 10(-9) substitutions per site per year; and the divergence of the two paralogs is traced to 90 MYA, coinciding with a period of the diversification of angiosperms. Given no codon usage bias in both genes, natural selection alone cannot account for the 6.4-fold differences in the nucleotide variation at synonymous sites between the two paralogs. Random processes resulting in different coalescence times, 3.65 MYA at AtHVA22d vs. 1.20 MYA at AtHVA22e, may have predominantly contributed to the evident differences of the genetic diversity. Partially nonoverlapping modes of expression between the two functional paralogs suggest a subfunctionalization hypothesis for explaining the fates of duplicate loci.     

Barley strigolactone signalling mutant hvd14.d reveals the role of strigolactones in abscisic acid-dependent response to drought

Strigolactones (SLs) are a group of plant hormones involved in many aspects of plant development and stress adaptation. Here, we investigated the drought response of a barley (Hordeum vulgare L.) mutant carrying a missense mutation in the gene encoding the SL-specific receptor HvD14. Our results clearly showed that hvd14.d mutant is hyper-sensitive to drought stress. This was illustrated by a lower leaf relative water content (RWC), impaired photosynthesis, disorganization of chloroplast structure, altered stomatal density and slower closure of stomata in response to drought in the mutant compared to the wild type parent cultivar Sebastian. Although the content of abscisic acid (ABA) and its derivatives remained unchanged in the mutant, significant differences in expression of genes related to ABA biosynthesis were observed. Moreover, hvd14.d was insensitive to ABA during seed germination. Analysis of Arabidopsis thaliana mutant atd14-1 also demonstrated that mutation in the SL receptor resulted in increased sensitivity to drought. Our results indicate that the drought-sensitive phenotype of barley SL mutant might be caused by a disturbed ABA metabolism and/or signalling pathways. These results together uncovered a link between SL signalling and ABA-dependent drought stress response in barley.     

紫花苜蓿赤霉素受体基因的克隆及表达分析

赤霉素受体(GID)是赤霉素信号转导途径的重要成员,直接影响着赤霉素对植物体效应的发挥。该研究利用同源克隆的方法,首次从紫花苜蓿中克隆得到1个赤霉素受体基因,命名为MsGID1b。序列分析发现,MsGID1b基因开放阅读框长度为1 053bp,编码350个氨基酸,推测其蛋白质分子量为39.839kD,是一个无信号肽和跨膜结构的亲水性蛋白。序列比对结果表明,MsGID1b基因与蒺藜苜蓿MtGID1b基因的核苷酸序列相似性为98%,氨基酸序列相似性为99%,且具有HSL家族典型的HGG和GXSXG保守结构域及GA、DELLA蛋白结合位点。荧光定量PCR分析表明,MsGID1b基因在紫花苜蓿各组织中的表达丰度依次为:根盛花初花茎叶荚果;经GA3、ABA、NaCl、PEG和黑暗诱导后该基因表达上调,尤其是在GA3诱导下,MsGID1b基因的表达量一直维持在较高水平,表明MsGID1b基因可能参与紫花苜蓿的抗逆调控。     

Arabidopsis EIN2 modulates stress response through abscisic acid response pathway

The nuclear protein ETHYLENE INSENSITIVE2 (EIN2) is a central component of the ethylene signal transduction pathway in plants, and plays an important role in mediating cross-links between several hormone response pathways, including abscisic acid (ABA). ABA mediates stress responses in plants, but there is no report on the role of EIN2 on plant response to salt and osmotic stresses. Here, we show that EIN2 gene regulates plant response to osmotic and salt stress through an ABA-dependent pathway in Arabidopsis. The expression of the EIN2 gene is down-regulated by salt and osmotic stress. An Arabidopsis EIN2 null mutant was supersensitive to both salt and osmotic stress conditions. Disruption of EIN2 specifically altered the expression pattern of stress marker gene RD29B in response to the stresses, but not the stress- or ABA-responsive genes RD29A and RD22, suggesting EIN2 modulates plant stress responses through the RD29B branch of the ABA response. Furthermore, disruption of EIN2 caused substantial increase in ABA. Lastly, our data showed that mutations of other key genes in ethylene pathway also had altered sensitivity to abiotic stresses, indicating that the intact ethylene may involve in the stress response. Taken together, the results identified EIN2 as a cross-link node in ethylene, ABA and stress signaling pathways, and EIN2 is necessary to induce developmental arrest during seed germination, and seedling establishment, as well as subsequent vegetative growth, thereby allowing the survival and growth of plants under the adverse environmental conditions. Youning Wang and Chuang Liu contributed equally to this work.     

蒙古沙冬青AmRD22基因的克隆及耐逆功能研究

脱水应答蛋白22(RD22)属于植物特有的BURP蛋白家族中的一个亚族,与耐逆性关系密切。该研究从中国西北荒漠区特有的强耐逆植物蒙古沙冬青克隆到一个RD22基因(AmRD22)的全长cDNA,并对其编码蛋白、表达模式和耐逆功能进行了研究。结果表明：(1)AmRD22蛋白(360 aa)的初级结构中含有RD22亚族共有的4个结构域,预测其定位于细胞壁;在功能已知的RD22蛋白中,AmRD22与大豆GmRD22的进化关系最近。(2)在室内培养的蒙古沙冬青幼苗中,AmRD22的表达受失水、高盐、低温和ABA胁迫的诱导显著上调,其中失水和低温胁迫诱导其上调幅度较大;在野外生长的蒙古沙冬青植株嫩叶中,其表达量从中秋至隆冬远高于其他季节。(3)转AmRD22基因拟南芥的耐盐性显著提高且Na⁺含量降低,其耐旱性也有较明显的改善且在种子萌发早期对外源ABA的敏感性降低,但耐冷性和耐冻性无明显变化。     

Dehydration-Stress-Regulated Transgene Expression in Stably Transformed Rice Plants

To confer abscisic acid (ABA) and/or stress-inducible gene expression, an ABA-response complex (ABRC1) from the barley (Hordeum vulgare L.) HVA22 gene was fused to four different lengths of the 5′ region from the rice (Oryza sativa L.) Act1 gene. Transient assay of β-glucuronidase (GUS) activity in barley aleurone cells shows that, coupled with ABRC1, the shortest minimal promoter (Act1–100P) gives both the greatest induction and the highest level of absolute activity following ABA treatment. Two plasmids with one or four copies of ABRC1 combined with the same Act1–100P and HVA22(I) of barley HVA22 were constructed and used for stable expression of uidA in transgenic rice plants. Three Southern blot-positive lines with the correct hybridization pattern for each construct were obtained. Northern analysis indicated that uidA expression is induced by ABA, water-deficit, and NaCl treatments. GUS activity assays in the transgenic plants confirmed that the induction of GUS activity varies from 3- to 8-fold with different treatments or in different rice tissues, and that transgenic rice plants harboring four copies of ABRC1 show 50% to 200% higher absolute GUS activity both before and after treatments than those with one copy of ABRC1.     

苹果SRS基因家族的鉴定与功能分析北大核心CSCD

SHI-related sequence(SRS)基因家族通过介导激素变化以调控植物成花及生长发育,并且在适应环境胁迫中起重要调控作用。该研究基于苹果(Malus domestica Borkh.)基因组数据,通过生物信息学手段鉴定苹果SRS基因家族成员,并分析SRS基因家族特点与功能及表达情况。结果表明:(1)苹果MdSRS基因家族共包含11个成员,分别命名为MdSRS1-MdSRS11,不均匀地分布在苹果的9条染色体上。(2)MdSRS蛋白包含229~414个不等的氨基酸残基,等电点分布在6.38~9.36之间;亚细胞定位结果表明,MdSRS蛋白大多分布于细胞膜,在细胞核、叶绿体中也有分布。(3)通过引入拟南芥、水稻、番茄及杨树的SRS基因进行系统发育分析表明,将11个MdSRSs分成5个亚族(A-A),在A4中分布最多。(4)顺式作用元件分析表明,11个MdSRSs启动子上游2 000 bp序列分布有激素、环境适应性和逆境诱导等响应元件。(5)荧光定量PCR结果显示,苹果MdSRS基因家族在盐胁迫和干旱胁迫下总体呈下调表达,在ABA胁迫后大多呈上调表达,是具有很大潜力的抗性候选基因,说明SRS家族对ABA调节等非生物胁迫具有调控作用。研究认为,SRS家族的11个成员均参与了调控干旱、盐及ABA胁迫多种逆境的响应,推测在实际苹果生产中对抵御不良环境具有重要作用。