Fruit development

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    Ripening and rot: How ripening processes influence disease susceptibility in fleshy fruits
    Shan Li, Yu Zhao, Pan Wu, Donald Grierson, Lei Gao
    J Integr Plant Biol 2024, 66 (9): 1831-1863.  
    doi: 10.1111/jipb.13739
    Abstract (Browse 64)  |   Save
    Fleshy fruits become more susceptible to pathogen infection when they ripen; for example, changes in cell wall properties related to softening make it easier for pathogens to infect fruits. The need for high-quality fruit has driven extensive research on improving pathogen resistance in important fruit crops such as tomato (Solanum lycopersicum). In this review, we summarize current progress in understanding how changes in fruit properties during ripening affect infection by pathogens. These changes affect physical barriers that limit pathogen entry, such as the fruit epidermis and its cuticle, along with other defenses that limit pathogen growth, such as preformed and induced defense compounds. The plant immune system also protects ripening fruit by recognizing pathogens and initiating defense responses involving reactive oxygen species production, mitogen-activated protein kinase signaling cascades, and jasmonic acid, salicylic acid, ethylene, and abscisic acid signaling. These phytohormones regulate an intricate web of transcription factors (TFs) that activate resistance mechanisms, including the expression of pathogenesis-related genes. In tomato, ripening regulators, such as RIPENING INHIBITOR and NON_RIPENING, not only regulate ripening but also influence fruit defenses against pathogens. Moreover, members of the ETHYLENE RESPONSE FACTOR (ERF) family play pivotal and distinct roles in ripening and defense, with different members being regulated by different phytohormones. We also discuss the interaction of ripening-related and defense-related TFs with the Mediator transcription complex. As the ripening processes in climacteric and non-climacteric fruits share many similarities, these processes have broad applications across fruiting crops. Further research on the individual contributions of ERFs and other TFs will inform efforts to diminish disease susceptibility in ripe fruit, satisfy the growing demand for high-quality fruit and decrease food waste and related economic losses.
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    DNA methylation controlling abscisic acid catabolism responds to light to mediate strawberry fruit ripening
    Yunfan Sun, Xiaofang Yang, Rongrong Wu, Shouzheng Lv, Yunduan Li, Haoran Jia, Yuying Yang, Baijun Li, Wenbo Chen, Andrew C. Allan, Guihua Jiang, Yan-Na Shi and Kunsong Chen
    J Integr Plant Biol 2024, 66 (8): 1718-1734.  
    doi: 10.1111/jipb.13681
    Abstract (Browse 53)  |   Save
    Phytohormones, epigenetic regulation and environmental factors regulate fruit ripening but their interplay during strawberry fruit ripening remains to be determined. In this study, bagged strawberry fruit exhibited delayed ripening compared with fruit grown in normal light, correlating with reduced abscisic acid (ABA) accumulation. Transcription of the key ABA catabolism gene, ABA 8′-hydroxylase FaCYP707A4, was induced in bagged fruit. With light exclusion whole genome DNA methylation levels were up-regulated, corresponding to a delayed ripening process, while DNA methylation levels in the promoter of FaCYP707A4 were suppressed, correlating with increases in transcript and decreased ABA content. Experiments indicated FaCRY1, a blue light receptor repressed in bagged fruit and FaAGO4, a key protein involved in RNA-directed DNA methylation, could bind to the promoter of FaCYP707A4. The interaction between FaCRY1 and FaAGO4, and an increased enrichment of FaAGO4 directed to the FaCYP707A4 promoter in fruit grown under light suggests FaCRY1 may influence FaAGO4 to modulate the DNA methylation status of the FaCYP707A4 promoter. Furthermore, transient overexpression of FaCRY1, or an increase in FaCRY1 transcription by blue light treatment, increases the methylation level of the FaCYP707A4 promoter, while transient RNA interference of FaCRY1 displayed opposite phenotypes. These findings reveal a mechanism by which DNA methylation influences ABA catabolism, and participates in light-mediated strawberry ripening.
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    A transcriptional cascade involving BBX22 and HY5 finely regulates both plant height and fruit pigmentation in citrus
    Jialing Fu, Li Liao, Jiajing Jin, Zhihao Lu, Juan Sun, Lizhi Song, Yue Huang, Shengjun Liu, Ding Huang, Yuantao Xu, Jiaxian He, Bin Hu, Yiqun Zhu, Fangfang Wu, Xia Wang, Xiuxin Deng, Qiang Xu
    J Integr Plant Biol 2024, 66 (8): 1752-1768.  
    doi: 10.1111/jipb.13719
    Abstract (Browse 50)  |   Save
    Dwarfing is a pivotal agronomic trait affecting both yield and quality. Citrus species exhibit substantial variation in plant height, among which internode length is a core element. However, the molecular mechanism governing internode elongation remains unclear. Here, we unveiled that the transcriptional cascade consisting of B-BOX DOMAIN PROTEIN 22 (BBX22) and ELONGATED HYPOCOTYL 5 (HY5) finely tunes plant height and internode elongation in citrus. Loss-of-function mutations of BBX22 in an early-flowering citrus (Citrus hindsii “SJG”) promoted internode elongation and reduced pigment accumulation, whereas ectopic expression of BBX22 in SJG, sweet orange (C. sinensis), pomelo (C. maxima) or heterologous expression of BBX22 in tomato (Solanum lycopersicum) significantly decreased internode length. Furthermore, exogenous application of gibberellin A3 (GA3) rescued the shortened internode and dwarf phenotype caused by BBX22 overexpression. Additional experiments revealed that BBX22 played a dual role in regulation internode elongation and pigmentation in citrus. On the one hand, it directly bound to and activated the expression of HY5, GA metabolism gene (GA2 OXIDASE 8, GA2ox8), carotenoid biosynthesis gene (PHYTOENE SYNTHASE 1, PSY1) and anthocyanin regulatory gene (Ruby1, a MYB DOMAIN PROTEIN). On the other hand, it acted as a cofactor of HY5, enhancing the ability of HY5 to regulate target genes expression. Together, our results reveal the critical role of the transcriptional cascade consisting of BBX22 and HY5 in controlling internode elongation and pigment accumulation in citrus. Unraveling the crosstalk regulatory mechanism between internode elongation and fruit pigmentation provides key genes for breeding of novel types with both dwarf and health-beneficial fortification in citrus.
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    The transcriptional control of LcIDL1-LcHSL2 complex by LcARF5 integrates auxin and ethylene signaling for litchi fruitlet abscission
    Xingshuai Ma, Zidi He, Ye Yuan, Zhijian Liang, Hang Zhang, Vilde Olsson Lalun, Zhuoyi Liu, Yanqing Zhang, Zhiqiang Huang, Yulian Huang, Jianguo Li and Minglei Zhao
    J Integr Plant Biol 2024, 66 (6): 1206-1226.  
    doi: 10.1111/jipb.13646
    Abstract (Browse 77)  |   Save
    At the physiological level, the interplay between auxin and ethylene has long been recognized as crucial for the regulation of organ abscission in plants. However, the underlying molecular mechanisms remain unknown. Here, we identified transcription factors involved in indoleacetic acid (IAA) and ethylene (ET) signaling that directly regulate the expression of INFLORESCENCE DEFICIENT IN ABSCISSION (IDA) and its receptor HAESA (HAE), which are key components initiating abscission. Specifically, litchi IDA-like 1 (LcIDL1) interacts with the receptor HAESA-like 2 (LcHSL2). Through in vitro and in vivo experiments, we determined that the auxin response factor LcARF5 directly binds and activates both LcIDL1 and LcHSL2. Furthermore, we found that the ETHYLENE INSENSITIVE 3-like transcription factor LcEIL3 directly binds and activates LcIDL1. The expression of IDA and HSL2 homologs was enhanced in LcARF5 and LcEIL3 transgenic Arabidopsis plants, but reduced in ein3 eil1 mutants. Consistently, the expressions of LcIDL1 and LcHSL2 were significantly decreased in LcARF5- and LcEIL3-silenced fruitlet abscission zones (FAZ), which correlated with a lower rate of fruitlet abscission. Depletion of auxin led to an increase in 1-aminocyclopropane-1-carboxylic acid (the precursor of ethylene) levels in the litchi FAZ, followed by abscission activation. Throughout this process, LcARF5 and LcEIL3 were induced in the FAZ. Collectively, our findings suggest that the molecular interactions between litchi AUXIN RESPONSE FACTOR 5 (LcARF5)-LcIDL1/LcHSL2 and LcEIL3-LcIDL1 signaling modules play a role in regulating fruitlet abscission in litchi and provide a long-sought mechanistic explanation for how the interplay between auxin and ethylene is translated into the molecular events that initiate abscission.
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    A signaling cascade mediating fruit trait development via phosphorylation-modulated nuclear accumulation of JAZ repressor
    Wei Wang, Jinyao Ouyang, Yating Li, Changsheng Zhai, Bing He, Huahan Si, Kunsong Chen, Jocelyn K. C. Rose and Wensuo Jia
    J Integr Plant Biol 2024, 66 (6): 1106-1125.  
    doi: 10.1111/jipb.13654
    Abstract (Browse 124)  |   Save
    It is generally accepted that jasmonate-ZIM domain (JAZ) repressors act to mediate jasmonate (JA) signaling via CORONATINE-INSENSITIVE1 (COI1)-mediated degradation. Here, we report a cryptic signaling cascade where a JAZ repressor, FvJAZ12, mediates multiple signaling inputs via phosphorylation-modulated subcellular translocation rather than the COI1-mediated degradation mechanism in strawberry (Fragaria vesca). FvJAZ12 acts to regulate flavor metabolism and defense response, and was found to be the target of FvMPK6, a mitogen-activated protein kinase that is capable of responding to multiple signal stimuli. FvMPK6 phosphorylates FvJAZ12 at the amino acid residues S179 and T183 adjacent to the PY residues, thereby attenuating its nuclear accumulation and relieving its repression for FvMYC2, which acts to control the expression of lipoxygenase 3 (FvLOX3), an important gene involved in JA biosynthesis and a diverse array of cellular metabolisms. Our data reveal a previously unreported mechanism for JA signaling and decipher a signaling cascade that links multiple signaling inputs with fruit trait development.
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    SlBEL11 regulates flavonoid biosynthesis, thus fine-tuning auxin efflux to prevent premature fruit drop in tomato
    Xiufen Dong, Xianfeng Liu, Lina Cheng, Ruizhen Li, Siqi Ge, Sai Wang, Yue Cai, Yang Liu, Sida Meng, Cai-Zhong Jiang, Chun-Lin Shi, Tianlai Li, Daqi Fu, Mingfang Qi and Tao Xu
    J Integr Plant Biol 2024, 66 (4): 749-770.  
    doi: 10.1111/jipb.13627
    Abstract (Browse 148)  |   Save
    Auxin regulates flower and fruit abscission, but how developmental signals mediate auxin transport in abscission remains unclear. Here, we reveal the role of the transcription factor BEL1-LIKE HOMEODOMAIN11 (SlBEL11) in regulating auxin transport during abscission in tomato (Solanum lycopersicum). SlBEL11 is highly expressed in the fruit abscission zone, and its expression increases during fruit development. Knockdown of SlBEL11 expression by RNA interference (RNAi) caused premature fruit drop at the breaker (Br) and 3d post-breaker (Br+3) stages of fruit development. Transcriptome and metabolome analysis of SlBEL11-RNAi lines revealed impaired flavonoid biosynthesis and decreased levels of most flavonoids, especially quercetin, which functions as an auxin transport inhibitor. This suggested that SlBEL11 prevents premature fruit abscission by modulating auxin efflux from fruits, which is crucial for the formation of an auxin response gradient. Indeed, quercetin treatment suppressed premature fruit drop in SlBEL11-RNAi plants. DNA affinity purification sequencing (DAP-seq) analysis indicated that SlBEL11 induced expression of the transcription factor gene SlMYB111 by directly binding to its promoter. Chromatin immunoprecipitation-quantitative polymerase chain reaction and electrophoretic mobility shift assay showed that S. lycopersicum MYELOBLASTOSIS VIRAL ONCOGENE HOMOLOG111 (SlMYB111) induces the expression of the core flavonoid biosynthesis genes SlCHS1, SlCHI, SlF3H, and SlFLS by directly binding to their promoters. Our findings suggest that the SlBEL11-SlMYB111 module modulates flavonoid biosynthesis to fine-tune auxin efflux from fruits and thus maintain an auxin response gradient in the pedicel, thereby preventing premature fruit drop.
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    Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits
    Yezi Xiang, Taikui Zhang, Yiyong Zhao, Hongjin Dong, Hongyi Chen, Yi Hu, Chien‐Hsun Huang, Jun Xiang and Hong Ma
    J Integr Plant Biol 2024, 66 (2): 228-251.  
    doi: 10.1111/jipb.13618
    Abstract (Browse 51)  |   Save
    Fruit functions in seed protection and dispersal and belongs to many dry and fleshy types, yet their evolutionary pattern remains unclear in part due to uncertainties in the phylogenetic relationships among several orders and families. Thus we used nuclear genes of 502 angiosperm species representing 231 families to reconstruct a well supported phylogeny, with resolved relationships for orders and families with previously uncertain placements. Using this phylogeny as a framework, molecular dating supports a Triassic origin of the crown angiosperms, followed by the emergence of most orders in the Jurassic and Cretaceous and their rise to ecological dominance during the Cretaceous Terrestrial Revolution. The robust phylogeny allowed an examination of the evolutionary pattern of fruit and ovary types, revealing a trend of parallel carpel fusions during early diversifications in eudicots, monocots, and magnoliids. Moreover, taxa in the same order or family with the same ovary type can develop either dry or fleshy fruits with strong correlations between specific types of dry and fleshy fruits; such associations of ovary, dry and fleshy fruits define several ovary-fruit “modules” each found in multiple families. One of the frequent modules has an ovary containing multiple ovules, capsules and berries, and another with an ovary having one or two ovules, achenes (or other single-seeded dry fruits) and drupes. This new perspective of relationships among fruit types highlights the closeness of specific dry and fleshy fruit types, such as capsule and berry, that develop from the same ovary type and belong to the same module relative to dry and fleshy fruits of other modules (such as achenes and drupes). Further analyses of gene families containing known genes for ovary and fruit development identified phylogenetic nodes with multiple gene duplications, supporting a possible role of whole-genome duplications, in combination with climate changes and animal behaviors, in angiosperm fruit and ovary diversification.
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    ClSnRK2.3 negatively regulates watermelon fruit ripening and sugar accumulation
    Jinfang Wang, Yanping Wang, Yongtao Yu, Jie Zhang, Yi Ren, Shouwei Tian, Maoying Li, Shengjin Liao, Shaogui Guo, Guoyi Gong, Haiying Zhang and Yong Xu
    J Integr Plant Biol 2023, 65 (10): 2336-2348.  
    DOI: 10.1111/jipb.13535
    Abstract (Browse 194)  |   Save
    Watermelon (Citrullus lanatus) as non-climacteric fruit is domesticated from the ancestors with inedible fruits. We previously revealed that the abscisic acid (ABA) signaling pathway gene ClSnRK2.3 might influence watermelon fruit ripening. However, the molecular mechanisms are unclear. Here, we found that the selective variation of ClSnRK2.3 resulted in lower promoter activity and gene expression level in cultivated watermelons than ancestors, which indicated ClSnRK2.3 might be a negative regulator in fruit ripening. Overexpression (OE) of ClSnRK2.3 significantly delayed watermelon fruit ripening and suppressed the accumulation of sucrose, ABA and gibberellin GA4. Furthermore, we determined that the pyrophosphate-dependent phosphofructokinase (ClPFP1) in sugar metabolism pathway and GA biosynthesis enzyme GA20 oxidase (ClGA20ox) could be phosphorylated by ClSnRK2.3 and thereby resulting in accelerated protein degradation in OE lines and finally led to low levels of sucrose and GA4. Besides that, ClSnRK2.3 phosphorylated homeodomain-leucine zipper protein (ClHAT1) and protected it from degradation to suppress the expression of the ABA biosynthesis gene 9’-cis-epoxycarotenoid dioxygenase 3 (ClNCED3). These results indicated that ClSnRK2.3 negatively regulated watermelon fruit ripening by manipulating the biosynthesis of sucrose, ABA and GA4. Altogether, these findings revealed a novel regulatory mechanism in non-climacteric fruit development and ripening.
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    Preferential transport activity of DkDTX5/MATE5 affects the formation of different astringency in persimmon
    Ying Liu, Xin Wu, Chenfeng Sun, Wenxing Chen, Meng Zhang, Niannian Liu, Qinglin Zhang, Liqing Xu and Zhengrong Luo
    J Integr Plant Biol 2023, 65 (10): 2304-2319.  
    DOI: 10.1111/jipb.13550
    Abstract (Browse 109)  |   Save
    Proanthocyanidins (PAs) are specialized metabolites that influence persimmon fruit quality. Normal astringent (A)-type and non-astringent (NA)-type mutants show significant variation in PA accumulation, but the influencing mechanism remains unclear. In this study, among the six identified DTXs/MATEs proteins associated with PA accumulation, we observed that allelic variation and preferential transport by DkDTX5/MATE5 induced variation in PA accumulation for A-type and NA-type fruit. The expression pattern of DkDTX5/MATE5 was correlated with PA accumulation in NA-type fruit. Upregulation and downregulation of DkDTX5/MATE5 promoted and inhibited PA accumulation, respectively, in the NA-type fruit. Interestingly, transporter assays of Xenopus laevis oocytes indicated that DkDTX5/MATE5 preferentially transported the PA precursors catechin, epicatechin, and epicatechin gallate, resulting in their increased ratios relative to the total PAs, which was the main source of variation in PA accumulation between the A-type and NA-type. The allele lacking Ser-84 in DkDTX5/MATE5 was identified as a dominantly expressed gene in the A-type and lost its transport function. Site-directed mutagenesis revealed that DkDTX5/MATE5 binds to PA precursors via Ser-84. These findings clarify the association between the transporter function of DkDTX5/MATE5 and PA variation, and can contribute to the breeding of new cultivars with improved fruit quality.
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    MaBEL1 regulates banana fruit ripening by activating cell wall and starch degradation-related genes
    Zunyang Song, Xiaoyang Zhu, Xiuhua Lai, Hangcong Chen, Lihua Wang, Yulin Yao, Weixin Chen and Xueping Li
    J Integr Plant Biol 2023, 65 (9): 2036-2055.  
    doi: 10.1111/jipb.13506
    Abstract (Browse 240)  |   Save
    Banana is a typical subtropical fruit, sensitive to chilling injuries and prone to softening disorder. However, the underlying regulatory mechanisms of the softening disorder caused by cold stress remain obscure. Herein, we found that BEL1-LIKE HOMEODOMAIN transcription factor 1 (MaBEL1) and its associated proteins regulate the fruit softening and ripening process. The transcript and protein levels of MaBEL1 were up-regulated with fruit ripening but severely repressed by the chilling stress. Moreover, the MaBEL1 protein interacted directly with the promoters of the cell wall and starch degradation-related genes, such as MaAMY3, MaXYL32, and MaEXP-A8. The transient overexpression of MaBEL1 alleviated fruit chilling injury and ripening disorder caused by cold stress and promoted fruit softening and ripening of “Fenjiao” banana by inducing ethylene production and starch and cell wall degradation. The accelerated ripening was also validated by the ectopic overexpression in tomatoes. Conversely, MaBEL1-silencing aggravated the chilling injury and ripening disorder and repressed fruit softening and ripening by inhibiting ethylene production and starch and cell wall degradation. MaABI5-like and MaEBF1, the two positive regulators of the fruit softening process, interacted with MaBEL1 to enhance the promoter activity of the starch and cell wall degradation-related genes. Moreover, the F-box protein MaEBF1 does not modulate the degradation of MaBEL1, which regulates the transcription of MaABI5-like protein. Overall, we report a novel MaBEL1-MaEBF1-MaABI5-like complex system that mediates the fruit softening and ripening disorder in “Fenjiao” bananas caused by cold stress.
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    The brassinosteroid signaling component SlBZR1 promotes tomato fruit ripening and carotenoid accumulation
    Fanliang Meng, Haoran Liu, Songshen Hu, Chengguo Jia, Min Zhang, Songwen Li, Yuanyuan Li, Jiayao Lin, Yue Jian, Mengyu Wang, Zhiyong Shao, Yuanyu Mao, Lihong Liu and Qiaomei Wang
    J Integr Plant Biol 2023, 65 (7): 1794-1813.  
    doi: 10.1111/jipb.13491
    Abstract (Browse 250)  |   Save
    The plant hormone ethylene is essential for climacteric fruit ripening, although it is unclear how other phytohormones and their interactions with ethylene might affect fruit ripening. Here, we explored how brassinosteroids (BRs) regulate fruit ripening in tomato (Solanum lycopersicum) and how they interact with ethylene. Exogenous BR treatment and increased endogenous BR contents in tomato plants overexpressing the BR biosynthetic gene SlCYP90B3 promoted ethylene production and fruit ripening. Genetic analysis indicated that the BR signaling regulators Brassinazole-resistant1 (SlBZR1) and BRI1-EMS-suppressor1 (SlBES1) act redundantly in fruit softening. Knocking out SlBZR1 inhibited ripening through transcriptome reprogramming at the onset of ripening. Combined transcriptome deep sequencing and chromatin immunoprecipitation followed by sequencing identified 73 SlBZR1-repressed targets and 203 SlBZR1-induced targets involving major ripening-related genes, suggesting that SlBZR1 positively regulates tomato fruit ripening. SlBZR1 directly targeted several ethylene and carotenoid biosynthetic genes to contribute to the ethylene burst and carotenoid accumulation to ensure normal ripening and quality formation. Furthermore, knock-out of Brassinosteroid-insensitive2 (SlBIN2), a negative regulator of BR signaling upstream of SlBZR1, promoted fruit ripening and carotenoid accumulation. Taken together, our results highlight the role of SlBZR1 as a master regulator of tomato fruit ripening with potential for tomato quality improvement and carotenoid biofortification.
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    The origin and evolution of carpels and fruits from an evo-devo perspective
    Hongyan Liu, Jun Li, Pichang Gong and Chaoying He
    J Integr Plant Biol 2023, 65 (2): 283-298.  
    doi: 10.1111/jipb.13351
    Abstract (Browse 282)  |   Save
    The flower is an evolutionary innovation in angiosperms that drives the evolution of biodiversity. The carpel is integral to a flower and develops into fruits after fertilization, while the perianth, consisting of the calyx and corolla, is decorative to facilitate pollination and protect the internal organs, including the carpels and stamens. Therefore, the nature of flower origin is carpel and stamen origin, which represents one of the greatest and fundamental unresolved issues in plant evolutionary biology. Here, we briefly summarize the main progress and key genes identified for understanding floral development, focusing on the origin and development of the carpels. Floral ABC models have played pioneering roles in elucidating flower development, but remain insufficient for resolving flower and carpel origin. The genetic basis for carpel origin and subsequent diversification leading to fruit diversity also remains elusive. Based on current research progress and technological advances, simplified floral models and integrative evolutionary-developmental (evo-devo) strategies are proposed for elucidating the genetics of carpel origin and fruit evolution. Stepwise birth of a few master regulatory genes and subsequent functional diversification might play a pivotal role in these evolutionary processes. Among the identified transcription factors, AGAMOUS (AG) and CRABS CLAW (CRC) may be the two core regulatory genes for carpel origin as they determine carpel organ identity, determinacy, and functionality. Therefore, a comparative identification of their protein–protein interactions and downstream target genes between flowering and non-flowering plants from an evo-devo perspective may be primary projects for elucidating carpel origin and development.
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    Methionine oxidation and reduction of the ethylene signaling component MaEIL9 are involved in banana fruit ripening
    Lisha Zhu, Lin Chen, Chaojie Wu, Wei Shan, Danling Cai, Zengxiang Lin, Wei Wei, Jianye Chen, Wangjin Lu, Jianfei Kuang
    J Integr Plant Biol 2023, 65 (1): 150-166.  
    doi: 10.1111/jipb.13363
    Abstract (Browse 251)  |   Save
    The ethylene insensitive 3/ethylene insensitive 3-like (EIN3/EIL) plays an indispensable role in fruit ripening. However, the regulatory mechanism that links post-translational modification of EIN3/EIL to fruit ripening is largely unknown. Here, we studied the expression of 13 MaEIL genes during banana fruit ripening, among which MaEIL9 displayed higher enhancement particularly in the ripening stage. Consistent with its transcript pattern, abundance of MaEIL9 protein gradually increased during the ripening process, with maximal enhancement in the ripening. DNA affinity purification (DAP)-seq analysis revealed that MaEIL9 directly targets a subset of genes related to fruit ripening, such as the starch hydrolytic genes MaAMY3D and MaBAM1. Stably overexpressing MaEIL9 in tomato fruit hastened fruit ripening, whereas transiently silencing this gene in banana fruit retarded the ripening process, supporting a positive role of MaEIL9 in fruit ripening. Moreover, oxidation of methionines (Met-129, Met-130, and Met-282) in MaEIL9 resulted in the loss of its DNA-binding capacity and transcriptional activation activity. Importantly, we identified MaEIL9 as a potential substrate protein of methionine sulfoxide reductase A MaMsrA4, and oxidation of Met-129, Met-130, and Met-282 in MaEIL9 could be restored by MaMsrA4. Collectively, our findings reveal a novel regulatory network controlling banana fruit ripening, which involves MaMsrA4-mediated redox regulation of the ethylene signaling component MaEIL9.
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    Transcriptional regulation of fleshy fruit texture
    Yanna Shi, Bai‐Jun Li, Guanqing Su, Mengxue Zhang, Donald Grierson and Kun‐Song Chen
    J Integr Plant Biol 2022, 64 (9): 1649-1672.  
    doi: 10.1111/jipb.13316
    Abstract (Browse 385)  |   Save

    Fleshy fruit texture is a critically important quality characteristic of ripe fruit. Softening is an irreversible process which operates in most fleshy fruits during ripening which, together with changes in color and taste, contributes to improvements in mouthfeel and general attractiveness. Softening results mainly from the expression of genes encoding enzymes responsible for cell wall modifications but starch degradation and high levels of flavonoids can also contribute to texture change. Some fleshy fruit undergo lignification during development and post-harvest, which negatively affects eating quality. Excessive softening can also lead to physical damage and infection, particularly during transport and storage which causes severe supply chain losses. Many transcription factors (TFs) that regulate fruit texture by controlling the expression of genes involved in cell wall and starch metabolism have been characterized. Some TFs directly regulate cell wall targets, while others act as part of a broader regulatory program governing several aspects of the ripening process. In this review, we focus on advances in our understanding of the transcriptional regulatory mechanisms governing fruit textural change during fruit development, ripening and post-harvest. Potential targets for breeding and future research directions for the control of texture and quality improvement are discussed.

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    Natural variation in the NAC transcription factor NONRIPENING contributes to melon fruit ripening
    Jinfang Wang, Shouwei Tian, Yongtao Yu, Yi Ren, Shaogui Guo, Jie Zhang, Maoying Li, Haiying Zhang, Guoyi Gong, Min Wang and Yong Xu
    J Integr Plant Biol 2022, 64 (7): 1448-1461.  
    DOI: 10.1111/jipb.13278
    Abstract (Browse 362)  |   Save

    The NAC transcription factor NONRIPENING (NOR) is a master regulator of climacteric fruit ripening. Melon (Cucumis melo L.) has climacteric and non-climacteric fruit ripening varieties and is an ideal model to study fruit ripening. Two natural CmNAC-NOR variants, the climacteric haplotype CmNAC-NORS,N and the non-climacteric haplotype CmNAC-NORA,S, have effects on fruit ripening; however, their regulatory mechanisms have not been elucidated. Here, we report that a natural mutation in the transcriptional activation domain of CmNAC-NORS,N contributes to climacteric melon fruit ripening. CmNAC-NOR knockout in the climacteric-type melon cultivar “BYJH” completely inhibited fruit ripening, while ripening was delayed by 5–8 d in heterozygous cmnac-nor mutant fruits. CmNAC-NOR directly activated carotenoid, ethylene, and abscisic acid biosynthetic genes to promote fruit coloration and ripening. Furthermore, CmNAC-NOR mediated the transcription of the “CmNAC-NOR-CmNAC73-CmCWINV2” module to enhance flesh sweetness. The transcriptional activation activity of the climacteric haplotype CmNAC-NORS,N on these target genes was significantly higher than that of the non-climacteric haplotype CmNAC-NORA,S. Moreover, CmNAC-NORS,N complementation fully rescued the non-ripening phenotype of the tomato (Solanum lycopersicum) cr-nor mutant, while CmNAC-NORA,S did not. Our results provide insight into the molecular mechanism of climacteric and non-climacteric fruit ripening in melon.

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    MdbHLH3 modulates apple soluble sugar content by activating phosphofructokinase gene expression
    Jian‐Qiang Yu, Kai‐Di Gu, Li‐Li Zhang, Cui‐Hui Sun, Quan‐Yan Zhang, Jia‐Hui Wang, Chu‐Kun Wang, Wen‐Yan Wang, Meng‐Chi Du and Da‐Gang Hu
    J Integr Plant Biol 2022, 64 (4): 884-900.  
    DOI: 10.1111/jipb.13236
    Abstract (Browse 255)  |   Save

    Sugars are involved in plant growth, fruit quality, and signaling perception. Therefore, understanding the mechanisms involved in soluble sugar accumulation is essential to understand fruit development. Here, we report that MdPFPβ, a pyrophosphate-dependent phosphofructokinase gene, regulates soluble sugar accumulation by enhancing the photosynthetic performance and sugar-metabolizing enzyme activities in apple (Malus domestica Borkh.). Biochemical analysis revealed that a basic helix-loop-helix (bHLH) transcription factor, MdbHLH3, binds to the MdPFPβ promoter and activates its expression, thus promoting soluble sugar accumulation in apple fruit. In addition, MdPFPβ overexpression in tomato influenced photosynthesis and carbon metabolism in the plant. Furthermore, we determined that MdbHLH3 increases photosynthetic rates and soluble sugar accumulation in apple by activating MdPFPβ expression. Our results thus shed light on the mechanism of soluble sugar accumulation in apple leaves and fruit: MdbHLH3 regulates soluble sugar accumulation by activating MdPFPβ gene expression and coordinating carbohydrate allocation.

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    Cited: Web of Science(12)
      
    Fig fruit ripening is regulated by the interaction between ethylene and abscisic acid
    Han Qiao, Han Zhang, Zhun Wang and Yuanyue Shen
    J Integr Plant Biol 2021, 63 (3): 553-569.  
    doi: 10.1111/jipb.13065
    Abstract (Browse 351)  |   Save
    Fleshy fruit ripening is typically regulated by ethylene in climacteric fruits and abscisic acid (ABA) in non‐climacteric fruits. Common fig (Ficus carica) shows a dual‐ripening mechanism, which is not fully understood. Here, we detected separate peaks of ethylene and ABA in fig fruits at the onset‐ and on‐ripening stages, in conjunction with a sharp rise in glucose and fructose contents. In a newly‐designed split‐fruit system, exogenous ethylene failed to rescue fluridone‐inhibited fruit ripening, whereas exogenous ABA rescued 2‐amino‐ethoxy‐vinyl glycine (AVG)‐inhibited fruit ripening. Transcriptome analysis revealed changes in the expression of genes key to both ABA and ethylene biosynthesis and perception during fig fruit ripening. At the de‐greening stage, downregulation of FcACO2 or FcPYL8 retarded ripening, but downregulation of FcETR1/2 did not; unexpectedly, downregulation of FcAAO3 promoted ripening, but it inhibited ripening only before the de‐greening stage. Furthermore, we detected an increase in ethylene emissions in the FcAAO3‐RNAi ripening fruit and a decrease in ABA levels in the FcACO2‐RNAi unripening fruit. Importantly, FcPYL8 can bind to ABA, suggesting that it functions as an ABA receptor. Our findings support the hypothesis that ethylene regulates the fig fruit ripening in an ABA‐dependent manner. We propose a model for the role of the ABA–ethylene interaction in climacteric/non‐climacteric processes.
    References   |   Full Text HTML   |   Full Text PDF   |   Cited By
      
    A PpEIL2/3–PpNAC1–PpWRKY14 module regulates fruit ripening by modulating ethylene production in peach
    Yudi Liu, Wen Xiao, Liao Liao, Beibei Zheng, Yunpeng Cao, Yun Zhao, Ruo-Xi Zhang, Yuepeng Han
    DOI: 10.1111/jipb.13761
    Version of Record online: 24 August 2024
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