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Reproductive biology of fruit and nut tree crops

Special Issue:
Reproductive biology of fruit and nut tree crops

Editor: Chitose Honsho and Tomoya Esumi
April 2022

The Japanese Society for Horticultural Science has published special issues of The Horticulture Journal (Hort. J.) to further enhance the value and attractiveness of this journal. The theme of the fourth special issue is “Reproductive biology of fruit and nut tree crops.”

Reproductive development in plant species involves a series of dynamic and interesting biological events. In fruit and nut tree crops, reproductive events are essential for fruit and nut production because the reproductive organs develop into edible parts and are a source of products. A comprehensive understanding of reproduction in fruit and nut tree crops will lead to the improvement of fruit productivity, the development of seedless fruit, the practical and technical improvement of pollination and fertilization, and others. On the other hand, some fruit tree crops have inherent barriers that interrupt fertilization for hybrid formation, such as self-incompatibility and male or female sterility, which are intriguing topics in the basic science of plant reproduction, and an understanding of those topics will contribute to the breeding and creation of new cultivars. In addition, ongoing climate changes, namely, global warming, have affected reproductive processes in perennial trees, ultimately influencing fruit and nut production. In this regard, the study of the physiology of reproductive development has become increasingly important in recent years from the perspective of coping with such environmental changes.

Research of the reproductive system and process in fruit and nut trees has long been pursued and remains active as one of the central topics in horticultural research. This special issue has been launched for the purpose of disseminating recent research outcomes from society members to the academic community of horticulture and fruit and nut industries worldwide.

 

REVIEW
Norimitsu Tanaka, Masato Wada

Pages: 91 (2): 131–139. 2022.|doi: 10.2503/hortj.UTD-R018

Abstract

Parthenocarpic apple cultivars have been recognized with simultaneous homeotic floral organ mutations. The mutations included replacements of petals to sepals and stamens to carpels, which were same as the class B mutations of floral organs from Arabidopsis and snapdragon. For apple, the parthenocarpy and class B mutations were tightly inherited and MdPISTILLATA (MdPI) gene deficiency caused homeotic mutations. However, the relationship between the suppression of MdPI and parthenocarpy was unclear. Transgenic apples with suppressed MdPI expression using an anti-sense or co-suppression method were found to have the same homeotic floral organ mutations as parthenocarpic cultivars. Further, the transformants with co-suppression showed parthenocarpy and overexpression of MdPI in fruits prevented normal fruit growth. Other apple MADS genes were analyzed for parthenocarpy. MdMADS13 is classified as another class B gene, which plays a role in floral organ formation together with MdPI. In addition, MdMADS1/8 and MdMADS9 are classified as class E genes, which are could function like SEP1 and 2 genes from Arabidopsis. The MdMADS1/8 and MdMADS9 gene-suppressed apple transformants showed strong inhibition of fruit enlargement, supporting the idea that MdMADS1/8 and MdMADS9 contribute to hypanthium development. It is possible that the MdPI, MdMADS13, MdMADS1/8, and MdMADS9 proteins formed a heterotetramer as a transcriptional regulator and were involved in fruit development. Other plant species such as tomato and grape also showed the respective class B genes affected fruit development. The suppression of tomato class B genes led to class B floral organ mutations and parthenocarpy, and a grape mutant with class B gene expression ectopically inhibited fruit flesh development. Both class B genes seemed to prevent fruit development similar to the apple MdPI. This suggests that the class B genes play not only a role in forming the identities of petals and stamens, but also a pivotal role in fruit development.


ORIGINAL ARTICLE
Kyoka Nagasaka, Hisayo Yamane, Soichiro Nishiyama, Shu Ebihara, Ryusuke Matsuzaki, Masakazu Shoji, Ryutaro Tao

Pages: 91 (2): 140–151. 2022.|doi: 10.2503/hortj.UTD-332

Abstract

Pollination is an important factor affecting fruit development in highbush blueberry (Vaccinium corymbosum L.). In general, planting several different blueberry cultivars increases the chances of cross-pollination and ensures high-quality fruit production. However, little is known about the effects of the pollen source on fruit development in blueberry. The aims of this study were: 1) to understand the effects of the pollen source on fruit size and quality; and 2) to explore the mechanisms underlying fruit development affected by the pollen source. We first characterized the pollination effect on fruit development using 14 different pollination combinations for several years and found that the number of mature seeds and fruit size differed significantly among the fruit pollinated by different pollen sources. Significant correlations between the number of mature seeds and fruit size were found in most combinations, whereas the number of mature seeds was not correlated with other fruit quality parameters such as sugar concentration. Our results and those of previous reports showed that the number of mature seeds, which was influenced by the pollen source, was a primary determinant of fruit size. Time-course observation during fruit development revealed that fruit weight and cell size significantly differed between self-pollinated and cross-pollinated fruit from 30 days after pollination onwards. To explore the molecular mechanisms underlying berry growth affected by developing seeds, we compared gene expression changes between self-pollinated and cross-pollinated fruit. Transcriptome analysis of fruit at 10 days after pollination suggested that auxin signaling pathways were enhanced in cross-pollinated fruit compared with self-pollinated fruit. We thus hypothesize that activated auxin signal transduction underlying early stage seed and fruit development may promote fruit cell enlargement during the early stage of fruit growth in highbush blueberry.


ORIGINAL ARTICLE
Panawat Sikhandakasmita, Ikuo Kataoka, Ryosuke Mochioka, Kenji Beppu

Pages: 91 (2): 152–156. 2022.|doi: 10.2503/hortj.UTD-341

Abstract

In protected agriculture, optimum temperature management is crucial for enhancing fruit productivity and maintaining cost-effective production. The aim of the present study was to investigate the effects of temperature on peach fruit development and quality. Container-grown ‘KU-PP2’ peach trees grafted on low-chill peach rootstocks were cultivated under controlled conditions at different temperatures (20, 25, and 30°C) during fruit development for two years (2020 and 2021). Fruit growth rates were calculated by measuring fruit diameter every 3 d from fruit setting to first harvest; fruit quality and phytochemistry were analyzed at harvest. Growing temperature markedly affected fruit growth, maturation, and fruit quality. The development of fruit in all treatments exhibited double sigmoid growth curves that included three stages (S1, S2, and S3). Fruit growth rate during S1 and S2 stages was increased, and fruit development period was significantly shortened with an increase in temperature. Contrary to the duration of S3, which was longer at higher temperatures, fruit grown at a high temperature (30°C) ripened by 12–18 days earlier than those grown at low-temperature regimes. In addition, high-temperature conditions were also associated with reduced fruit quality (size, weight, and sweetness), but enhanced development of red coloration. Therefore, even though high-temperature conditions can accelerate early fruit expansion and hasten fruit maturity, such conditions also have negative effects on important agronomic fruit traits.


ORIGINAL ARTICLE
Soichiro Nishiyama, Daisuke Yoshimura, Akihiko Sato, Keizo Yonemori

Pages: 91 (2): 157–168. 2022.|doi: 10.2503/hortj.UTD-333

Abstract

Gibberellins are widely used to induce seedlessness in table grape production, but are not effective for every cultivar or developmental stage. In order to characterize the potential physiological mechanism behind gibberellin-induced seedlessness, we conducted tissue-specific transcriptome analysis of ovules and ovaries from cultivars with different levels of receptiveness to seedlessness induction. GA3 treatment at full bloom highly induced gibberellin signaling and various phytohormone signaling pathway genes in ovules at two days after treatment, but had less effect in ovaries, which suggests that GA3 directly affects seed development. During the development to six days after GA3 application, cell cycle-related genes in the ovules were markedly downregulated, indicating that this may be related to ovule abortion induction. The marked transcriptomic responses were largely absent in a cultivar with low receptiveness to gibberellin-induced seedlessness, suggesting a crucial role for the observed tissue-specific responses in the successful induction of seedlessness by GA3 application. Collectively, our transcriptome analysis highlights distinct tissue-specific reactions to GA3 during early berry development, providing important insights for the successful production of seedless berries by gibberellin application.


ORIGINAL ARTICLE
Yan Wang, Hao Wang, Jing Zhang, Zhen-Shan Liu, Qing Chen, Wen He, Shao-Feng Yang, Yuan-Xiu Lin, Yun-Ting Zhang, Meng-Yao Li, Yong Zhang, Ya Luo, Hao-Ru Tang, Xiao-Rong Wang

Pages: 91 (3): 267–275. 2022.|doi: 10.2503/hortj.UTD-331

Abstract

The Chinese cherry (Prunus pseudocerasus/Cerasus pseudocerasus), which is native to China, is an economically important tetraploid fruiting cherry species. Its industry has been greatly limited due to some general disadvantages in the fruits such as small fruit size, high acid content, and short shelf-life. As such, it is urgent to carry out cross breeding and genetic improvement of this species. Here, seven cross combinations were designed by selecting five genotype landraces of the Chinese cherry and one semi-wild resource as cross parents. The fruit-set percentage, germination rate of the hybrid seeds, and growth status of the F1 seedlings varied among different parental genotypes and cross combinations. Three or four S-genotypes were detected in six tetraploid parents, with a maximum of five different alleles between two parents. Both the pollen vigor of the male parent and the differential S-genotype between parents may contribute to the variation in fruit-set percentages, ranging from 0 to 28.55%. Significant differences in the F0 fruit traits were observed among different combinations, indicating potential metaxenia of the Chinese cherry. Appropriate pretreatments, including the removal of endocarps, soaking with 150 mg/L GA3 for 24 h, and chilling stratification for 7–10 days, could significantly increase the germination rate of the hybrid seeds. According to the overall performance, using (semi)-wild resources as one of the parents should be taken into consideration more in Chinese cherry breeding programs. On the basis of these findings, we further constructed a flow chart for successful intra-specific crossing and efficient cultivation of robust F1 seedlings. This study will provide important references for the selection of cross parents, establishment of a feasible breeding program, and cultivation of robust F1 progenies of the Chinese cherry.


ORIGINAL ARTICLE
Yoshihiro Takemura, Keisuke Tochimoto, Takushi Yoshida, Mutsuki Kitamura, Shotaro Wada, Sakie Takazawa, Toshihiko Inamoto, Fumio Tamura

Pages: 91 (3): 276–285. 2022.|doi: 10.2503/hortj.UTD-339

Abstract

Low temperature negatively affects pollen germination in many species, but artificial pollination can help alleviate these negative effects. With ongoing environmental changes, it is important to select pollinizers with pollen that has superior germination properties at lower temperatures. To select candidate cultivars for a new Pyrus pollinizer for pollen with superior germination properties at low temperatures, in vitro pollen germination was studied in 129 Pyrus plants. The highest germination percentage for most Pyrus plants was observed at 25.0°C and was < 20% at 10.0°C. However, ‘Narayoshinokoboku’, ‘Imamuranatsu’, and ‘Tosanashi’ showed a higher germination rate than the other Pyrus plants at 10.0°C, and the germination percentage rates of three plants were > 30%. The fruit setting percentage of the cultivars ‘Kosui’, ‘Hosui’, and ‘Gold-Nijisseiki’ were > 85% by pollination using these three selected cultivars in an open field. In addition, S-genotyping in selected cultivars was determined as follows: ‘Tosanashi’ (S1S7), ‘Imamuranatsu’ (S1S12), and ‘Narayoshinokoboku’ (S1S9). From these results, we concluded that all three cultivars showed cross-compatibility in most pear cultivars of the four major Japanese pear cultivars. The percentage of flower bud formation in ‘Tosanashi’ was > 50%, and the amount of pollen from ‘Narayoshinokoboku’ was more than double the amount of ‘Chojuro’. By assessing the chilling requirement in selected cultivars, a safe area for growth for each cultivar was evaluated as all areas with the exception of the Kyushu and Shikoku regions, based on the ongoing progress of global warming (average daily temperature increase of 3.7°C). In conclusion, we selected ‘Narayoshinokoboku’ and ‘Tosanashi’ as new Pyrus pollinizers because they combine the advantages of low-temperature germinability and high pollen load.


ORIGINAL ARTICLE
Chitose Honsho, Ryuto Sakamoto, Shuji Ishimura, Takuya Tetsumura

Pages: 91 (3): 286–295. 2022.|doi: 10.2503/hortj.UTD-335

Abstract

This study was conducted to obtain insights into unreduced gamete formation in Citrus tamurana hort. ex Tanaka ‘Nishiuchi Konatsu’ and ‘Hyuganatsu’, inferred from unreduced pollen and egg cell genotype information. To establish a method for fine genotyping of tissues with higher ploidy levels (up to hexaploidy), we first identified heterozygous single-nucleotide polymorphism (SNP) markers (CiC4240-04 and CiC5327-03) with close genetic distance to centromeres of ‘Nishiuchi Konatsu’ and ‘Hyuganatsu’. Fluorescence intensity-based standard plots were generated using real-time qPCR to accurately genotype these SNP markers on a two-dimensional panel. Ten normal seeds were obtained from fertilization of unreduced gametes by self-pollination of ‘Nishiuchi Konatsu’ or ‘Hyuganatsu’ × ‘Nishiuchi Konatsu’ crosses. Inner seed coats with hexaploid endosperm tissues and tetraploid embryos were obtained from normal seeds, and their CiC4240-04 and CiC5327-03 genotypes were determined with standard plots using real-time qPCR. Genotypes of unreduced pollen and egg cells were uniquely determined from the genotype information of 6x endosperms and 4x embryos, and the unreduced gamete formation process was inferred. The results showed that unreduced pollen formation was almost entirely due to first division restitution (FDR); therefore, it was concluded that FDR was the dominant formation process for unreduced pollen in ‘Nishiuchi Konatsu’. In contrast, there was no dominant process for the formation of unreduced egg cells because both FDR and second division restitution occurred in almost the same number of individuals with unreduced egg cells.


ORIGINAL ARTICLE
Takumi Arakawa, Shinji Kamio, Masahiko Yamada

Pages: 91 (3): 296–301. 2022.|doi: 10.2503/hortj.UTD-344

Abstract

Large nut weight (NW) is an important target in chestnut breeding. The present study was conducted at the Nakatsugawa branch of the Gifu Prefectural Research Institute for Agricultural Technology, an important chestnut breeding site in Japan. We estimated the environmental variance components for NW by using nine cultivars/selections with three single-tree replicates for six years. The number of nuts evaluated for each tree was mostly over 100 nuts, with an average of 440 nuts. Subsequently, the dataset of average NW values for each tree was log-transformed and analyzed by ANOVA. The effects of genotype, year, and the genotype × year interactions were highly significant, whereas the tree effect was negligible. The resulting environmental variance components for the log-transformed values were as follows: variance among years = 5.2 × 10−4, variance among trees within genotype = 0, variance associated with the genotype × year interactions = 7.6 × 10−4, and residual variance = 11.2 × 10−4. The results suggest that tree replication is not necessary to evaluate the genotypic value of cultivars/selections or offspring in breeding and that year effect adjustment and yearly repeated measurements can effectively reduce environmental variance. The NW of 27 cultivars/selections with potential as cross-parents was also estimated with no tree replications and via measurements repeated for three years; the results ranged from 10.7 to 47.4 g, with high broad-sense heritability (0.93) based on a three-year evaluation for the log-transformed data. Based on the environmental variance estimates, the cultivars/selections used in chestnut breeding with NW above 22.3 and 26.7 g should be selected by evaluating one tree for three years at 95% probability and selecting those having nuts of 25 and 30 g or more, respectively.


ORIGINAL ARTICLE
Yutaro Osako, Hisayo Yamane, Ryunhee Kim, Hisashi Miyagawa, Ryutaro Tao

Pages: 91 (3): 302–311. 2022.|doi: 10.2503/hortj.UTD-352

Abstract

Seed size affects the edible portion rate of lychee fruit and is therefore an important trait for fruit quality in lychee (Litchi chinensis). Lychee fruits can be classified into four categories in terms of seed properties: normal, small, aborted seed and seedless. ‘Salathiel’ is known to bear a relatively high rate of aborted-seeded (pseudo-parthenocarpy, stenospermocarpy) and seedless (parthenocarpy) fruit regardless of environmental and cultivation conditions. In other horticultural fruit crops, such as tomato, auxin metabolism and signaling is critical for parthenocarpy, although auxin metabolism has not been characterized in relation to (pseudo) parthenocarpy in lychee. The purpose of this study was to characterize the physiological and morphological properties of maternal reproductive organs in ‘Salathiel’ female flowers, with a specific focus on the associated auxin metabolism. Microscopic observations of the internal structures of the ‘Salathiel’ embryo revealed that ‘Salathiel’ reproductive organ differentiation is similar to that of normal-seeded cultivars. However, the obturator was significantly smaller in ‘Salathiel’ than in other normal-seeded cultivars, suggesting that specific developmental characteristics may exist in the maternal reproductive organs of ‘Salathiel’. Our investigation of indole acetic acid (IAA) contents revealed that IAA levels were significantly higher in ‘Salathiel’ than in other cultivars. Moreover, the IAA metabolite contents also differed significantly between ‘Salathiel’ and the normal-seeded and small-seeded cultivars. Specifically, N-3-hydroxy-2-oxindole-3-acetyl glutamic acid contents were significantly higher in ‘Salathiel’ than in ‘Yu Her Pau’ and ‘Hei Ye’. 3-hydroxy-2-oxindole-3-acetic acid was lower in ‘Yu Her Pau’ and ‘Salathiel’ than in ‘Hei Ye’, while indole-acetylaspartic acid was significantly lower in ‘Salathiel’ compared to ‘Hei Ye’. Expression analyses of the genes related to auxin biosynthesis, catabolism, transport, and signaling indicated that the IAA influx-related and efflux-related gene expression levels were respectively higher and lower in ‘Salathiel’ than in the other cultivars, which is consistent with the increased IAA accumulation in the ‘Salathiel’ ovary. The possible involvement of auxin metabolism in the aborted-seeded and seedless fruit production in ‘Salathiel’ is discussed herein.


ORIGINAL ARTICLE
Ayako Katayama-Ikegami, Yuta Sugiyama, Takane Katayama, Akiko Sakamoto, Ryo Shimada, Chiho Miyazaki, Mei Gao-Takai

Pages: 91 (3): 312–321. 2022.|doi: 10.2503/hortj.UTD-342

Abstract

Changes in anthocyanin and endogenous abscisic acid (ABA) contents in the berry skins of Vitis labruscana × V. vinifera cultivars, ‘Aki Queen’, and ‘Ruby Roman’ were investigated during the fruit development period. Color development of ‘Aki Queen’ berries mainly occurred within 20 days post véraison, while that of the ‘Ruby Roman’ was prolonged for about 40 days. In both cultivars, the ABA level in the berry skin started to increase a few days before véraison; however, ABA accumulation ceased approximately 10 days after véraison in ‘Aki Queen’, while it continued until the late stage of maturation in ‘Ruby Roman’. In addition, higher indole-3-acetate aspartate (IAA-Asp) and lower isopentenyladenine (iP) contents were observed in ‘Ruby Roman’ than in ‘Aki Queen’ at the late development stage. The expression analysis of genes involved in ABA metabolism revealed that V. vinifera 9-cis-epoxycarotenoid dioxygenase 3 (VviNCED3), which is assumed to play a major role in ABA biosynthesis, remained relatively higher in ‘Ruby Roman’ than in ‘Aki Queen’ after véraison. Considering that ABA plays a regulatory role in grape maturation, these results may indicate that the coloration of ‘Ruby Roman’ at the later stage of maturation is partly attributable to an increased ABA pool in berry skins.


ORIGINAL ARTICLE
Daiki Matsumoto, Seita Shimizu, Aoi Shimazaki, Kohei Ito, Satoshi Taira

Pages: 91 (4): 432–436. 2022.|doi: 10.2503/hortj.UTD-385

Abstract

Akebia trifoliata is cultivated locally in few areas of Japan. Artificial pollination is considered indispensable for stable fruit production, as Akebia spp. exhibit self-incompatibility (SI). However, little is known about the reproductive physiology required for effective artificial pollination. In this study, we investigated the effects of self-pollen contamination on the fruit set of ‘Fuji Murasaki’ (A. trifoliata), one of the main lines in Yamagata Prefecture, Japan. Both the self- and cross-pollen tubes reached the base of the ovary and penetrated the ovules at 10 days after pollination, indicating that A. trifoliata exhibits late-acting SI. Self-pollination one day before cross-pollination completely inhibited fruit set, while self-pollination one day after cross-pollination did not inhibit fruit set in both 2016 and 2020, indicating interference in cross-pollination by self-pollen contamination. Fruit set rates for artificial pollination using a 1:1 mix of self- and cross-pollen were significantly lower than those that used non-contaminated cross-pollen in both 2016 and 2019, but were comparable when using a 1:1 mix of lycopodium powder and cross-pollen. The seed number of fruit resulting from mixed pollination was not significantly lower than that of fruit resulting from cross-pollination. Interestingly, 1:1 mixed pollination of self- and cross-pollen sometimes yielded abnormal fruits with an apex that remained pale and did not soften. These results suggest that excessive self-pollen contamination in artificial pollination may not be desirable for A. trifoliata fruit production.


ORIGINAL ARTICLE
Kentaro Ono, Kaho Masui, Ryutaro Tao

Pages: 91 (4): 437–447. 2022.|doi: 10.2503/hortj.QH-002

Abstract

Prunus (Rosaceae) includes many commercially important fruit crop species that exhibit self-incompatibility (SI), including sweet cherry (P. avium L.), Japanese apricot (P. mume Sieb. et Zucc.), Japanese plum (P. salicina Lindl.), apricot (P. armeniaca L.), and almond (P. dulcis [Mill.] D. A. Webb.). These species exhibit S-ribonuclease-based gametophytic SI, which prevents self-pollen tube growth in the pistil. The successful production of self-fertilized progeny accomplished by artificially overcoming the SI barrier has not been reported in Prunus, but self-compatible (SC) Prunus mutants with mutated pollen S determinant S haplotype–specific F-box (SFB) or pollen modifier M-locus encoded glutathione S-transferase-like (MGST) genes have been identified and used as SC cultivars and breeding stocks. In this study, we suppressed translation of SFB or MGST mRNA in self-pollen using antisense oligonucleotides to overcome the SI barrier in P. avium, P. mume, and P. salicina. Over the three years of the study, we obtained self-fertilized progeny of SI Japanese plum ‘Sordum’ only when SFB or MGST was knocked down. We also found that the average length of the self-pollinated pollen tube in the pistil of ‘Sordum’ was increased following treatment with an antisense oligonucleotide against SFB. This is the first report regarding the successful production of selfed progeny of Prunus obtained by disrupting SI. Our findings also provide evidence that the loss of function of SFB or MGST in Prunus pollen leads to SC.


ORIGINAL ARTICLE
Tomohiro Kondo, Hana Morizono

Pages: 91 (4): 448–452. 2022.|doi: 10.2503/hortj.QH-006

Abstract

To determine the effects of drought stress, especially light drought stress, on flower number in passion fruit, one-year-old passion fruit plants grown in 7.5 L plastic pots were subjected to different soil water content treatments, namely wetness, light drought, and heavy drought for two months. Average, maximum, and minimum soil water contents (v/v) were 44, 47, and 41% in the wetness treatment, 23, 40, and 11% in the light drought treatment and 11, 33, and 6% in the heavy drought treatment. Flower number decreased as the strength of drought stress increased, although the number of nodes and flower buds did not. Flowering periods were from June 27 to July 19 in the wetness treatment and June 26 to July 16 in the light drought treatment with three peaks around July 1, 6, and 13. In the heavy drought treatment, the flowering period was from July 11 to 18 with one peak. The flower bud number was not affected by drought stress. Light drought stress did not suppress vegetative growth, such as vine length, leaf number, leaf length, or photosynthetic rate, although heavy drought stress did. Stomatal conductance was suppressed by light drought only at 12:00PM and by heavy drought throughout the day. Leaf water potential was decreased by heavy drought at 3:00PM, but not by light drought. In the wetness and light drought treatments, visible wilting was not observed, and in the heavy drought treatment the plants wilted before irrigation, although they recovered about 15 min after irrigation. In conclusion, even light drought stress, which did not suppress vegetative growth, reduced the flower number in passion fruit. Drought stress suppressed flower bud development but not differentiation.

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