Self-sterility May Be Due to Prezygotic Late-acting Self-incompatibility and Early-acting Inbreeding Depression in Chinese Chestnut

Xiong, Huan; Feng, Zhaozhong; Guo, Sheng; Yuan, Deyi; Niu, Genhua

doi:10.21273/jashs04634-18

Cited by 25 publications

(27 citation statements)

References 40 publications

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“…Chestnut trees are characterized by massive blooming, huge pollen production and the largest pollen:ovule ratio ever reported in plants (Larue et al 2021a). They are characterized by multiple and complex mechanisms that limit self-pollination (Xiong et al 2019; Larue et al 2022). At the flower level, chestnuts are monoecious: they have separate male and female flowers.…”

Section: Methodsmentioning

confidence: 99%

Harmful self-pollination drives gynodioecy in European chestnut, a self-incompatible tree

Larue

Petit

2022

Preprint

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Background and Aim: In gynodioecious plants, male-sterile individuals must have a female advantage to coexist with bisexual individuals. In European chestnuts, characterized by a form of late-acting self-incompatibility, male-fertile trees produce large amounts of pollen when female flowers are receptive, resulting in abundant self-pollination. Here we study whether male-sterile chestnut trees have an increased fruit set compared to male-fertile trees because they escape from the negative consequences of self-pollination on ovules, a case of self-interference. Methods: We measured fruit set of 242 male-fertile and male-sterile trees during three consecutive years. To test experimentally the hypothesis of negative interference of self-pollen on ovules as the origin of the female advantage of male-sterile trees, we emasculated male-fertile trees and compared their fruit set with that of control male-fertile trees. We performed the same experiment on male-sterile trees by removing the sterile but rewarding male catkins as a natural control to test for the effect of decreased insect attractiveness on fruit set. Key Results: The fruit set of male-sterile trees is higher than that of male-fertile trees by a factor of two in some years. Following emasculation, male-fertile trees have a higher fruit set than control male-fertile trees, pointing to a negative effect of the massive amount of self-pollen produced by fertile male catkins on fertilization probability of female flowers. In contrast, emasculated male-sterile trees had a lower fruit set than control male-sterile trees, pointing to a decrease in insect attractiveness after removing nectar-producing male catkins. Conclusions: Our emasculation experiment showed that sexual interference results in massive ovule discounting in male-fertile trees, sufficient for accounting for the persistence of female trees in natural populations of European chestnut trees.

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Section: Methodsmentioning

confidence: 99%

Harmful self-pollination drives gynodioecy in European chestnut, a self-incompatible tree

Larue

Petit

2022

Preprint

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“…Thus, the low number of seeds with embryos in fruits from self-pollination in this species is not directly related (or is not the only determinant) to the SI mechanism, but rather to inbreeding depression [ 27 ]. The self-incompatibility and inbreeding depression action in the same individual has been recorded mainly in species with pre-zygotic LSI [ 4 , 28 , 29 ] in which the ovule fertilization high rate after self-pollination is due to a failure in the SI system. Thus, the inbreeding depression is the cause of seed abortion after self-pollination in A. johannensis [ 27 ], which is a phenomenon that we can confirm in other partially self-incompatible Pleurothallidinae species, as reported by Borba et al [ 8 , 9 ].…”

Section: Discussionmentioning

confidence: 99%

Two Self-Incompatibility Sites Occur Simultaneously in the Same Acianthera Species (Orchidaceae, Pleurothallidinae)

Duarte

Oliveira

Borba

2020

Plants

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In most species of Pleurothallidinae, the self-incompatibility site occurs in the stylar canal inside the column, which is typical of gametophytic self-incompatibility (GSI). However, in some species of Acianthera, incompatible pollen tubes with anomalous morphology reach the ovary, as those are obstructed in the column. We investigated if a distinct self-incompatibility (SI) system is acting on the ovary of A. johannensis, which is a species with partial self-incompatibility, contrasting with a full SI species, A. fabiobarrosii. We analyzed the morphology and development of pollen tubes in the column, ovary, and fruit using light, epifluorescence, and transmission electron microscopy. Our results show that the main reaction site in A. johannensis is in the stylar canal inside the column, which was also recorded in A. fabiobarrosii. Morphological and cytological characteristics of the pollen tubes with obstructed growth in the column indicated a process of programmed cell death in these tubes, showing a possible GSI reaction. In addition, partially self-incompatible individuals of A. johannensis exhibit a second SI site in the ovary. We suggest that this self-incompatibility site in the ovary is only an extension of GSI that acts in the column, differing from the typical late-acting self-incompatibility system recorded in other plant groups.

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“…While the SI of rosaceous fruit trees is stylar type, the SI of A. quinata is reported to be LSI (Kawagoe and Suzuki, 2005). A few fruit trees are also known to exhibit LSI, such as chestnut (Castanea mollissima) (Fagaceae), durian (Durio zibethinus) (Malvaceae), and feijoa (Acca sellowiana) (Myrtaceae), although the detailed mechanisms are still unknown (Finatto et al, 2011;Honsho et al, 2004;Lo et al, 2007;Xiong and Zou, 2019). The characteristic feature of LSI is that self-pollen competes with crosspollen for ovule and/or fruit set in several species (Gibbs, 2014;Seavey and Bawa, 1986).…”

Section: Introductionmentioning

confidence: 99%

Effects of Self-pollen Contamination in Artificial Pollination on Fruit Set of ‘Fuji Murasaki’ <i>Akebia trifoliata</i>

et al. 2022

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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. Selfpollination 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.

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Self-sterility May Be Due to Prezygotic Late-acting Self-incompatibility and Early-acting Inbreeding Depression in Chinese Chestnut

Cited by 25 publications

References 40 publications

Harmful self-pollination drives gynodioecy in European chestnut, a self-incompatible tree

Harmful self-pollination drives gynodioecy in European chestnut, a self-incompatible tree

Two Self-Incompatibility Sites Occur Simultaneously in the Same Acianthera Species (Orchidaceae, Pleurothallidinae)

Effects of Self-pollen Contamination in Artificial Pollination on Fruit Set of ‘Fuji Murasaki’ <i>Akebia trifoliata</i>

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