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Authors: Jianhong Hu, Xiao Li and Tai-ping Sun.
Nature Plants (2023)
Editor's view: Mutant combinations of four AUXIN RESPONSE FACTORs in tomato by CRISPR–Cas9 technology reveal their dual function in inhibiting fruit set before pollination while activating fruit growth after fertilization.
Abstract: "In flowering plants, auxin produced in seeds after fertilization promotes fruit initiation. The application of auxin to unpollinated ovaries can also induce parthenocarpy (seedless fruit production). Previous studies have shown that auxin signalling components SlIAA9 and SlARF7 (a class A AUXIN RESPONSE FACTOR (ARF)) are key repressors of fruit initiation in tomato (Solanum lycopersicum). A similar repressive role of class A ARFs in fruit set has also been observed in other plant species. However, evidence is lacking for a role of any class A ARF in promoting fruit development as predicted in the current auxin signalling model. Here we generated higher-order tomato mutants of four class A SlARFs (SlARF5, SlARF7, SlARF8A and SlARF8B) and uncovered their precise combinatorial roles that lead to suppressing and promoting fruit development. All four class A SlARFs together with SlIAA9 inhibited fruit initiation but promoted subsequent fruit growth. Transgenic tomato lines expressing truncated SlARF8A/8B lacking the IAA9-interacting PB1 domain displayed strong parthenocarpy, further confirming the promoting role of SlARF8A/8B in fruit growth. Altering the doses of these four SlARFs led to biphasic fruit growth responses, showing their versatile dual roles as both negative and positive regulators. RNA-seq and chromatin immunoprecipitation–quantitative PCR analyses further identified SlARF8A/8B target genes, including those encoding MADS-BOX transcription factors (AG1, MADS2 and AGL6) that are key repressors of fruit set. These results support the idea that SlIAA9/SlARFs directly regulate the transcription of these MADS-BOX genes to inhibit fruit set. Our study reveals the previously unknown dual function of four class A SlARFs in tomato fruit development and illuminates the complex combinatorial effects of multiple ARFs in controlling auxin-mediated fruit set and fruit growth."
Authors: C. Mesejo, A. Martínez-Fuentes, C. Reig and M. Agustí.
Scientia Horticulturae (2022)
Highlights: • ‘Orri’ mandarin has a low parthenocarpic ability, in accordance with its low CcGA3ox1 gene expression, but the application of GA3 does not increase fruit set. • Ringing branches performed 35-40 days after anthesis increases fruitlet growth rate. This effect correlates inversely with the fruitlet abscission rate, and positively with cell division, i.e., with the CcCYCA1.1 gene expression in the fruitlet, but not with the GA biosynthesis, i. e., with the CcGA3ox1 gene expression. • Ringing branches significantly increased CcPIN1 gene expression in the fruitlet. • Results suggest that ringing protects the fruitlet abscission zone mediated by polar auxin transport from the fruit, which allows the fruitlet to maintain carbohydrate assimilation and continue growing.
Abstract: "Ringing branches is a technique which is widely used to increase the yield of Citrus cultivars with low parthenocarpic ability. When performed during the physiological fruitlet abscission stage it prevents fruitlet drop and increases the number of fruits harvested. This effect has been related with an increased carbohydrate supply, which requires an enhanced photosynthesis efficiency of leafy flowering shoots. Since ringing also reduces vegetative growth, both the number of shoots and the leaves per shoot, the mechanism by which the carbohydrate supply is increased should be revised. Our results show that ringing carried out at this stage maintains the ability of the ovary for cell division mediated by the availability of carbohydrates, as indicated by an increased CcCYCA1.1 expression. But this effect is not linked with an increase in GA1 biosynthesis (CcGA3ox1 expression), as this occurs during fruit set; hence, hormones other than gibberellin must be controlling the physiological fruitlet abscission in response to ringing. We found that an increased expression of the auxin efflux carrier CcPIN1 gene suggests that ringing induces the auxin export out of the fruitlet and transport to the abscission zone (AZ-C), thus inhibiting its activation and allowing carbohydrates supply to the fruitlet which, thus, prevents abscission and continues growth."
Authors: Miyako Kusano, Kanjana Worarad, Atsushi Fukushima,Ken Kamiya, Yuka Mitani, Yozo Okazaki, Yasuhiro Higashi, Ryo Nakabayashi, Makoto Kobayashi, Tetsuya Mori, Tomoko Nishizawa, Yumiko Takebayashi, Mikiko Kojima, Hitoshi Sakakibara, Kazuki Saito, Shuhei Hao, Yoshihito Shinozaki, Yoshihiro Okabe, Junji Kimbara,Tohru Ariizumi and Hiroshi Ezura.
Cells (2022)
Abstract: "Parthenocarpy, the pollination-independent fruit set, can raise the productivity of the fruit set even under adverse factors during the reproductive phase. The application of plant hormones stimulates parthenocarpy, but artificial hormones incur extra financial and labour costs to farmers and can induce the formation of deformed fruit. This study examines the performance of parthenocarpic mutants having no transcription factors of SlIAA9 and SlTAP3 and sldella that do not have the protein-coding gene, SlDELLA, in tomato (cv. Micro-Tom). At 0 day after the flowering (DAF) stage and DAFs after pollination, the sliaa9 mutant demonstrated increased pistil development compared to the other two mutants and wild type (WT). In contrast to WT and the other mutants, the sliaa9 mutant with pollination efficiently stimulated the build-up of auxin and GAs after flowering. Alterations in both transcript and metabolite profiles existed for WT with and without pollination, while the three mutants without pollination demonstrated the comparable metabolomic status of pollinated WT. Network analysis showed key modules linked to photosynthesis, sugar metabolism and cell proliferation. Equivalent modules were noticed in the famous parthenocarpic cultivars ‘Severianin’, particularly for emasculated samples. Our discovery indicates that controlling the genes and metabolites proffers future breeding policies for tomatoes.
Authors: Weifeng Chen, Zhengcao Xiao, Yule Wang, Jinxiao Wang, Rui Zhai, Kui Lin-Wang, Richard Espley, Fengwang Ma and Pengmin Li.
Horticulture Research (2021)
Abstract: "Flavonoids play important roles in regulating plant growth and development. In this study, three kaempferol 3-O-glycosides were identified and mainly accumulated in flowers but not in leaves or fruits of Malus. In Malus, flower petal color is normally white, but some genotypes have red flowers containing anthocyanin. Anthocyanin biosynthesis appears to be in competition with kaempferol 3-O-glycosides production and controlled by the biosynthetic genes. The white flower Malus genotypes had better-developed seeds than the red flower genotypes. In flowers, the overexpression of MYB10 in Malus domestica enhanced the accumulation of anthocyanin, but decreased that of kaempferol 3-O-glycosides. After pollination the transgenic plants showed slower pollen tube growth and fewer developed seeds. Exogenous application of different flavonoid compounds suggested that kaempferol 3-O-glycosides, especially kaempferol 3-O-rhamnoside, regulated pollen tube growth and seed set rather than cyanidin or quercetin 3-O-glycosides. It was found that kaempferol 3-O-rhamnoside might regulate pollen tube growth through effects on auxin, the Rho of plants (ROP) GTPases, calcium and the phosphoinositides signaling pathway. With the inhibition of auxin transport, the transcription levels of Heat Shock Proteins (HSPs) and ROP GTPases were downregulated while the levels were not changed or even enhanced when blocking calcium signaling, suggesting that HSPs and ROP GTPases were downstream of auxin signaling, but upstream of calcium signaling. In summary, kaempferol glycoside concentrations in pistils correlated with auxin transport, the transcription of HSPs and ROP GTPases, and calcium signaling in pollen tubes, culminating in changes to pollen tube growth and seed set."
Authors: Christian Clepet, Ravi Sureshbhai Devani, Rachid Boumlik, Yanwei Hao, Halima Morin, Fabien Marcel, Marion Verdenaud, Brahim Mania, Gwilherm Brisou, Sylvie Citerne, Gregory Mouille, Jean-Christophe Lepeltier, Shai Koussevitzky, Adnane Boualem and Abdelhafid Bendahmane.
Molecular Plant (2021)
Abstract: "Fruit set is inhibited by adverse temperatures, with consequences on yield. We isolated a tomato mutant producing fruits under non-permissive hot temperatures and identified the causal gene as SlHB15A, belonging to class-III homeodomain leucine-zipper transcription factors (HD-ZipIII). SlHB15A loss-of-function mutants display aberrant ovule development that mimics transcriptional changes occurring in fertilized ovules and leads to parthenocarpic fruit set under optimal and non-permissive temperatures, in field and glasshouse conditions. Under cold growing condition, SlHB15A is subjected to conditional haploinsufficiency and recessive dosage sensitivity controlled by microRNA 166 (miR166). Knockdown of SlHB15A alleles by miR166 leads to a continuum of aberrant ovules correlating with parthenocarpic fruit set. Consistent with this, plants harboring SlHB15A-miRNA166 resistant allele developed normal ovules and were unable to set parthenocarpic fruit under cold condition. DNA affinity purification sequencing (DAP-seq) and RNAseq analyses revealed SlHB15A is a bifunctional transcription factor, expressing in the ovule integument. SlHB15A binds to the promoters of auxin genes to repress auxin signaling and to ethylene genes to activate their expression. Survey of tomato genetic biodiversity identified pat and pat-1, two historical parthenocarpic mutants, as alleles of SlHB15A. Our finding demonstrates the role of SlHB15A as a sentinel to prevent fruit set in the absence of fertilization and provides a mean to enhance fruiting under extreme temperatures."
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Authors: Alon Israeli, Ramona Schubert, Nave Man, Naama Teboul, Juan Carlos Serrani Yarce, Emily E. Rosowski, Miin-Feng Wu, Matan Levy, Idan Efroni, Karin Ljung, Bettina Hause, Jason W. Reed and Naomi Ori.
Plant Physiology (2023)
Abstract: "Fruit formation depends on successful fertilization and is highly sensitive to weather fluctuations that affect pollination. Auxin promotes fruit initiation and growth following fertilization. Class A auxin response factors (Class A ARFs) repress transcription in the absence of auxin and activate transcription in its presence. Here we explore how multiple members of the ARF family regulate fruit set and fruit growth in tomato (Solanum lycopersicum) and Arabidopsis thaliana, and test whether reduction of SlARF activity improves yield stability in fluctuating temperatures. We found that several tomato Slarf mutant combinations produced seedless parthenocarpic fruits, most notably mutants deficient in SlARF8A and SlARF8B genes. Arabidopsis Atarf8 mutants deficient in the orthologous gene had less complete parthenocarpy than did tomato Slarf8a Slarf8b mutants. Conversely, Atarf6 Atarf8 double mutants had reduced fruit growth after fertilization. AtARF6 and AtARF8 likely switch from repression to activation of fruit growth in response to a fertilization-induced auxin increase in gynoecia. Tomato plants with reduced SlARF8A and SlARF8B gene dosage had substantially higher yield than the wild type under controlled or ambient hot and cold growth conditions. In field trials, partial reduction in the SlARF8 dose increased yield under extreme temperature with minimal pleiotropic effects. The stable yield of the mutant plants resulted from a combination of early onset of fruit set, more fruit-bearing branches and more flowers setting fruits. Thus, ARF8 proteins mediate the control of fruit set, and relieving this control with Slarf8 mutations may be utilized in breeding to increase yield stability in tomato and other crops."
Authors: Yunhe Tian, Wei Xin, Juncheng Lin, Jun Ma, Jun He, Xuhui Wang, Tongda Xu and Wenxin Tang.
Frontiers in Plant Science (2022)
Abstract: "In strawberries, fruit set is considered as the transition from the quiescent ovary to a rapidly growing fruit. Auxin, which is produced from the fertilized ovule in the achenes, plays a key role in promoting the enlargement of receptacles. However, detailed regulatory mechanisms for fruit set and the mutual regulation between achenes and receptacles are largely unknown. In this study, we found that pollination promoted fruit development (both achene and receptacle), which could be stimulated by exogenous auxin treatment. Interestingly, auxin was highly accumulated in achenes, but not in receptacles, after pollination. Further transcriptome analysis showed that only a small portion of the differentially expressed genes induced by pollination overlapped with those by exogenous auxin treatment. Auxin, but not pollination, was able to activate the expression of growth-related genes, especially in receptacles, which resulted in fast growth. Meanwhile, those genes involved in the pathways of other hormones, such as GA and cytokinin, were also regulated by exogenous auxin treatment, but not pollination. This suggested that pollination was not able to activate auxin responses in receptacles but produced auxin in fertilized achenes, and then auxin might be able to transport or transduce from achenes to receptacles and promote fast fruit growth at the early stage of fruit initiation. Our work revealed a potential coordination between achenes and receptacles during fruit set, and auxin might be a key coordinator."
Authors: Lü-Meng Liu, Han-Qing Zhang, Kun Cheng and Yuan-Ming Zhang.
Frontiers in Plant Science (2021)
Abstract: "There is limited advancement on seed number per pod (SNPP) in soybean breeding, resulting in low yield in China. To address this issue, we identified PIN1 and CKX gene families that regulate SNPP in Arabidopsis, analyzed the differences of auxin and cytokinin pathways, and constructed interaction networks on PIN1, CKX, and yield-related genes in soybean and cowpea. First, the relative expression level (REL) of PIN1 and the plasma membrane localization and phosphorylation levels of PIN1 protein were less in soybean than in cowpea, which make auxin transport efficiency lower in soybean, and its two interacted proteins might be involved in serine hydrolysis, so soybean has lower SNPP than cowpea. Then, the CKX gene family, along with its positive regulatory factor ROCK1, had higher REL and less miRNA regulation in soybean flowers than in cowpea ones. These lead to higher cytokinin degradation level, which further reduces the REL of PIN1 and decreases soybean SNPP. We found that VuACX4 had much higher REL than GmACX4, although the two genes essential in embryo development interact with the CKX gene family. Next, a tandem duplication experienced by legumes led to the differentiation of CKX3 into CKX3a and CKX3b, in which CKX3a is a key gene affecting ovule number. Finally, in the yield-related gene networks, three cowpea CBP genes had higher RELs than two soybean CBP genes, low RELs of three soybean-specific IPT genes might lead to a decrease in cytokinin synthesis, and some negative and positive SNPP regulation were found, respectively, in soybean and cowpea. These networks may explain the SNPP difference in the two crops. We deduced that ckx3a or ckx3a ckx6 ckx7 mutants, interfering CYP88A, and over-expressed DELLA increase SNPP in soybean. This study reveals the molecular mechanism for the SNPP difference in the two crops, and provides an important idea for increasing soybean yield."
Authors: Francisca Godoy, Nathalie Kühn, Mindy Muñoz, Germán Marchandon, Satyanarayana Gouthu, Laurent Deluc, Serge Delrot, Virginie Lauvergeat and Patricio Arce-Johnson.
Horticulture Research (2021)
Abstract: "Auxin is a key phytohormone that modulates fruit formation in many fleshy fruits through the regulation of cell division and expansion. Auxin content rapidly increases after pollination and the manipulation in its levels may lead to the parthenocarpic development. ln Vitis vinifera L., little is known about the early fruit development that encompasses from pollination to fruit set. Pollination/fertilization events trigger fruit formation, and auxin treatment mimics their effect in grape berry set. However, the role of auxin in this process at the molecular level is not well understood. To elucidate the participation of auxin in grapevine fruit formation, morphological, reproductive, and molecular events from anthesis to fruit set were described in sequential days after pollination. Exploratory RNA-seq analysis at four time points from anthesis to fruit set revealed that the highest percentage of genes induced/repressed within the hormone-related gene category were auxin-related genes. Transcript profiling showed significant transcript variations in auxin signaling and homeostasis-related genes during the early fruit development. Indole acetic acid and several auxin metabolites were present during this period. Finally, application of an inhibitor of auxin action reduced cell number and the mesocarp diameter, similarly to unpollinated berries, further confirming the key role of auxin during early berry development. This work sheds light into the molecular features of the initial fruit development and highlights the auxin participation during this stage in grapevine."
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