ArticlePublisher preview available

Analysis on the biological basis of stamen abortion during the second flowering of Magnolia × soulangeana ‘Changchun’

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract and Figures

Key message Stamen degeneration and meiosis failure during the second flowering of ‘Changchun’ were mainly attributed to the coordinated regulation of hormone metabolism, environmental temperature, and genetic factors. Abstract Magnolia × soulangeana ‘Changchun’, a woody ornamental plant, blossoms twice a year after once flower bud differentiation, with fertile flower buds in spring and sterile flower buds in summer. The phenotype of stamens of ‘Changchun’ in summer displays a decrease in length and width, and no pollen, thus aborting. Cytological evidence exhibited that the microspore mother cells in anthers failed to complete meiosis during summer flowering. Compared with spring flowering period, the contents of endogenous substances and hormones decreased in summer, such as IAA/GA, ABA/GA, IAA/ABA hormone ratios also changed, indicating that energy and substances needed for stamen development in summer were insufficient, and hormone balance was broken. Transcriptome data showed that there were 46,230 differentially expressed genes (DEGs) between spring and summer flower buds, including 19,816 up-regulated genes and 26,414 down-regulated genes. Further analysis identified that most of the significantly enriched DEGs were involved in DNA, nucleus, microtubules and other GO items related to meiosis process, which was mutually confirmed with cytological results, suggesting that abnormal meiosis may be the core problem of fertility decline of stamen in summer flower buds of ‘Changchun’. Besides, genes related to hormone signaling and heat stress that may affect stamen development were also differentially expressed. This study provided a basis for further understanding the stamen abortion mechanism of ‘Changchun’, and also provided a reference for exploring the fertility regulation of woody ornamental plants.
This content is subject to copyright. Terms and conditions apply.
Vol.:(0123456789)
1 3
Trees (2022) 36:1515–1528
https://doi.org/10.1007/s00468-022-02306-z
ORIGINAL ARTICLE
Analysis onthebiological basis ofstamen abortion duringthesecond
flowering ofMagnolia × soulangeana ‘Changchun
TangjieNie1· ZhengJiang1· LiyongSun1· YaoChen1· JiaLi1· AixiangYang1· ZengfangYin1
Received: 28 November 2021 / Accepted: 12 April 2022 / Published online: 16 May 2022
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022
Abstract
Key message Stamen degeneration and meiosis failure during the second flowering of ‘Changchun’ were mainly
attributed to the coordinated regulation of hormone metabolism, environmental temperature, and genetic factors.
Abstract Magnolia × soulangeana ‘Changchun’, a woody ornamental plant, blossoms twice a year after once flower bud dif-
ferentiation, with fertile flower buds in spring and sterile flower buds in summer. The phenotype of stamens of ‘Changchun
in summer displays a decrease in length and width, and no pollen, thus aborting. Cytological evidence exhibited that the
microspore mother cells in anthers failed to complete meiosis during summer flowering. Compared with spring flowering
period, the contents of endogenous substances and hormones decreased in summer, such as IAA/GA, ABA/GA, IAA/ABA
hormone ratios also changed, indicating that energy and substances needed for stamen development in summer were insuf-
ficient, and hormone balance was broken. Transcriptome data showed that there were 46,230 differentially expressed genes
(DEGs) between spring and summer flower buds, including 19,816 up-regulated genes and 26,414 down-regulated genes.
Further analysis identified that most of the significantly enriched DEGs were involved in DNA, nucleus, microtubules and
other GO items related to meiosis process, which was mutually confirmed with cytological results, suggesting that abnormal
meiosis may be the core problem of fertility decline of stamen in summer flower buds of ‘Changchun’. Besides, genes related
to hormone signaling and heat stress that may affect stamen development were also differentially expressed. This study
provided a basis for further understanding the stamen abortion mechanism of ‘Changchun’, and also provided a reference
for exploring the fertility regulation of woody ornamental plants.
Keywords Differentially expressed genes· Magnolia × soulangeana ‘Changchun’· Second flowering· Stamen abortion·
Transcriptome sequencing
Introduction
In nature, most plants bloom only once in a certain breed-
ing season of the year, but there are always exceptions,
some species of trees may flower more than once a year.
Second flowering refers to the phenomenon that the flower
buds formed by the differentiation of plants that originally
bloom only once a year open in the same year, resulting
in flowers twice a year (Wang and Wang 2009). It has
been recognized as a serious threat to fruit production due
to causing reduced fruit yield, thereby attracting much
attention in fruit cultivation (Kingston etal. 1990). For
ornamental plants, flower is one of the important orna-
mental traits, and second flowering enhances ornamental
and creates breathtaking beauty to our life instead (Guo
etal. 2017). Notably, second flowering is often accompa-
nied by abortion. In Pyrus pyrifolia, the second flower-
ing exhibits shorter filament, smaller petal size and much
higher abortive rate in comparison to the normal flowering
(Zhang 2015). However, previous studies tend to explain
the mechanism underlying the second flowering but not
flower abortion (Zhou etal. 2013; Jiang etal. 2019, 2020),
in spite of that reducing floral organ fertility of ornamen-
tal plants can effectively prolong the ornamental period
(Wei etal. 2019). Here, how to understand the biological
Communicated by J. Lin .
Tangjie Nie, Zheng Jiang contributed equally to this work.
* Zengfang Yin
zfyin@njfu.edu.cn
1 Co-Innovation Center forSustainable Forestry inSouthern
China, College ofBiology andtheEnvironment, Nanjing
Forestry University, Nanjing210037, China
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... The counting of the number of structures as well as the observation of particular characters need to be carried out during particular developmental phases for both male and female parts. Several chemical studies on the stamens of Magnolia species show their importance both in releasing the aroma (Wang et al. 2011) and in understanding stamen development (Nie et al. 2022). It is important to highlight that the stamens of Magnolia section Talauma are deciduous in the male phase and shed easily, a known characteristic of the genus that aims to better disperse pollen, being a highly specialized evolution (Figlar and Nooteboom 2004;Canright 1952). ...
Article
Full-text available
The genus Magnolia (Magnoliaceae) has a wide and disjunct geographic distribution ranging from Eastern and South Asia to Malaysia, extending across the Neartics and reaching into the Neotropics. Regarding its infrageneric classification, the genus is divided into three subgenera: Yulania , Gynopodium and Magnolia , the latter including the section Talauma in which the native Brazilian taxa are classified. The species of Magnolia sect. Talauma can be recognized by two parallel longitudinal scars on the petiole formed by the shedding of the stipules, in addition to a woody syncarp that breaks into irregular plates at dehiscence. Currently, in Brazil, species recognition is not clear on national platforms that are widely used by the Brazilian botanical community (e.g. Flora do Brasil), with only two native Magnolia species being accepted: M. amazonica and M. ovata . The lack of knowledge about the species and their respective characteristics has resulted in many identification errors in Brazilian herbaria, which contributes to the lack of knowledge about their current conservation status. We conducted a complete taxonomic revision based on extensive fieldwork, a herbarium survey, along with literature study. Based on this, we propose to recognize three previously described species, supporting the acceptance of five native Magnolias occurring in Brazil, namely: M. amazonica , M. brasiliensis , M. irwiniana , M. ovata and M. sellowiana . However, we follow the Flora do Brasil in maintaining M. paranaensis as a synonym of M. ovata . Additionally, we designate a lectotype for M. sellowiana . We present morphological descriptions and the geographic distribution for each species, in addition to an identification key to all of these plus the two introduced ornamental species from Asia and North America, illustrations, photographs, ecological data, updated conservation status and taxonomic notes.
... Magnolia soulangeana Soul.-Bod. is a kind of greening plant that originates in China and is widely transplanted and cultivated in Asia, North America, and South America (Lu et al., 2022), and its flowers have very high ornamental value (Firakova et al., 2008;Nie et al., 2022). Studies have found that its flowers are rich in essential oils, alkaloids, flavonoids, sugars, proteins, dietary fiber, starch, and other substances (Ziyaev et al., 1999;Wang et al., 2019), which has significant research significance for exploring its medicinal value and food value. ...
Article
This study innovatively designed a microwave-assisted hydrodistillation method with uniform heating to extract the essential oil from the withered flowers of Magnolia soulangeana Soul.-Bod., in which the addition of the rotating unit is applied to improve the uneven heating of plant materials caused by the fixation of the flask and the energy point in the microwave system, and the soaking pretreatment unit is used to fully swell the plant cells and accelerate the overflow of essential oils. Meanwhile, the significance of the independent variables that may affect the yield of essential oil and the optimal conditions were screened and optimized by means of response surface methodology, and the results showed that the introduction of the rotation unit and soaking pretreatment unit increased the yield of essential oil by 16.67% and 20%, respectively, which highly promoted the increase of the yield and extraction rate of essential oil. Moreover, the samples obtained by this new method are rich in terpene compounds, such as eucalyptol, δ-cadinene, α-muurolene, and germacrene D, which is consistent with the results of traditional hydrodistillation, and also further illustrates the safety of this method. And the hypolipidemic activity of these compounds was also verified, and the main compound in the essential oil that exerts the hypolipidemic activity may be δ-cadinene, and its possible target for reducing total cholesterol content is Niemann-Pick C1-like 1. In addition, this study also shows that this new method shows lower energy consumption and environmental pressure and is very promising to replace the existing method for the large-scale preparation of essential oils.
Article
Full-text available
Sea Island cotton is the best quality tetraploid cultivated cotton in the world, in terms of fiber quality. Glyphosate is a widely used herbicide in cotton production, and the improper use of herbicides has led to pollen abortion in sea island cotton and, consequently, to a dramatic decrease in yield; however, the mechanism remains unclear. In this study, different concentrations (0, 3.75, 7.5, 15, and 30 g/L) of glyphosate were applied to CP4-EPSPS transgenic sea island cotton Xinchang 5 in 2021 and 2022 at Korla, with 15 g/L glyphosate chosen as the suitable concentration. By comparing the paraffin sections of 2–24 mm anthers in the 15 g/L glyphosate treatment group with those in the water control group, we showed that the key period of anther abortion after glyphosate treatment was the formation and development of tetrads, which corresponded to 8–9 mm buds. Transcriptome sequencing analysis of the treated and control anthers revealed a significant enrichment of differentially expressed genes in phytohormone-related pathways, in particular abscisic acid response and regulation pathways. Additionally, after treatment with 15 g/L of glyphosate, there was a significant increase in the amount of abscisic acid in the anthers in the 8–9 mm buds. Further analysis of the differential expression of abscisic acid response and regulatory genes, an abscisic acid response gene GbTCP14 (Gbar_A11G003090) was identified, which was significantly upregulated in buds with 15 g/L glyphosate treatment than the control, and it could be a key candidate gene for the subsequent research involving male sterility induced by glyphosate in sea island cotton.
Article
Full-text available
Flowering is crucial to plant reproduction and controlled by multiple factors. However, the mechanisms underlying the regulation of flowering in perennial plants are still largely unknown. Here, we first report a super long blooming 1 (slb1) mutant of the relict tree Liriodendron chinense possessing a prolonged blooming period of more than 5 months, in contrast to the 1 month blooming period in the wild type (WT). Phenotypic characterization showed that earlier maturation of lateral shoots was caused by accelerated axillary bud fate, leading to the phenotype of continuous flowering in slb1 mutants. The transcriptional activity of genes related to hormone signaling (auxin, cytokinin, and strigolactone), nutrient availability, and oxidative stress relief further indicated active outgrowth of lateral buds in slb1 mutants. Interestingly, we discovered a unique FT splicing variant with intron retention specific to slb1 mutants, representing a potential causal mutation in the slb1 mutants. Surprisingly, most slb1 inbred offspring flowered precociously with shorter juvenility (~4 months) than that (usually 8–10 years) required in WT plants, indicating heritable variation underlying continuous flowering in slb1 mutants. This study reports an example of a perennial tree mutant that flowers continuously, providing a rare resource for both breeding and genetic research.
Article
Full-text available
Background Male sterility (MS) has important applications in hybrid seed production, and the abortion of anthers has been observed in many plant species. While most studies have focused on the genetic factors affecting male sterility, the dynamic gene expression patterns of pollen abortion in male sterile lines have not been fully elucidated. In addition, there is still no hybrid oat that is commercially planted due to the lack of a suitable system of male sterility for hybrid breeding. Results In this study, we cultivated a male sterile oat line and a near-isogenic line by crossbreeding to elucidate the expression patterns of genes that may be involved in sterility. The first reported CA male sterile (CAMS) oat line was used for cross-testing and hybridization experiments and was confirmed to exhibit a type of nuclear sterility controlled by recessive genes. Oat stamens of two lines were sampled at four different developmental stages separately. Paired-end RNA sequencing was performed for each sample and generated 252.84 Gb sequences. There were 295,462 unigenes annotated in public databases in all samples, and we compared the histological characteristics and transcriptomes of oat stamens from the two oat lines at different developmental stages. Our results demonstrate that the sterility of the male sterile oat line occurs in the early stage of stamen development and is primarily attributable to abnormal meiosis and the excessive accumulation of superoxide. Conclusions To the best of our knowledge, this study is the first to decipher the dynamic expression profiles of pollen abortion CAMS and CA male fertile (CAMF) oat lines, which may represent a valuable resource for further studies attempting to understand pollen abortion and anther development in oats.
Article
Full-text available
Background: Cytoplasmic male sterility (CMS) plays a crucial role in the utilization of heterosis and various types of CMS often have different abortion mechanisms. Therefore, it is important to understand the molecular mechanisms related to anther abortion in wheat, which remain unclear at present. Results: In this study, five isonuclear alloplasmic male sterile lines (IAMSLs) and their maintainer were investigated. Cytological analysis indicated that the abortion type was identical in IAMSLs, typical and stainable abortion, and the key abortive period was in the binucleate stage. Most of the 1,281 core shared differentially expressed genes identified by transcriptome sequencing compared with the maintainer in the vital abortive stage were involved in the metabolism of sugars, oxidative phosphorylation, phenylpropane biosynthesis, and phosphatidylinositol signaling, and they were downregulated in the IAMSLs. Key candidate genes encoding chalcone--flavonone isomerase, pectinesterase, and UDP-glucose pyrophosphorylase were screened and identified. Moreover, further verification elucidated that due to the impact of downregulated genes in these pathways, the male sterile anthers were deficient in sugar and energy, with excessive accumulations of ROS, blocked sporopollenin synthesis, and abnormal tapetum degradation. Conclusions: Through comparative transcriptome analysis, an intriguing core transcriptome-mediated male-sterility network was proposed and constructed for wheat and inferred that the downregulation of genes in important pathways may ultimately stunt the formation of the pollen outer wall in IAMSLs. These findings provide insights for predicting the functions of the candidate genes, and the comprehensive analysis of our results was helpful for studying the abortive interaction mechanism in CMS wheat.
Article
Full-text available
Litsea cubeba (Lour.) Pers., a popular essential oil plant, is a dioecious species with degenerative sexual organs in both male and female individuals. Yet, the mechanism of degenerative organs development in male and female flowers is poorly understood. Here, we analyzed the morphological characters of degenerative organ development by morphological and histological observations, and determined the critical stage of abortion that occurs at pre-meiosis in male and female flowers. We also conducted RNA sequencing (RNA-seq) to understand the genetic basis of stamen abortion in female flowers. The differentially expressed genes (DEGs) were identified during the staminode development in female flowers; functional enrichment analysis revealed some important biological pathways involved the regulation of stamen abortion, including plant hormone signal transduction, phenylpropanoid biosynthesis, flavonoid biosynthesis and monoterpenoid biosynthesis. Furthermore, 15 DEGs involved in the hormone pathways were found to regulate stamen development. By HPLC-MS/MS analysis, there were a salicylic acid (SA) content peak and the gibberellin (GA) content lowest point in the abortion processes in female flowers, suggesting a vital function of hormonal processes. Co-expression network analysis further identified several hub genes that potentially played significant roles in the stamen abortion of L. cubeba. Taken together, we proposed a model involved in plant hormones pathways underlying stamen abortion during pre-meiosis in female flowers of L. cubeba.
Article
Full-text available
Magnolia × soulangeana ‘Changchun’ are trees that bloom in spring and summer respectively after flower bud differentiation. Here, we use phenological and morphological observation and RNA-seq technology to study the molecular basis of flowering initiation in ‘Changchun’. During the process of flowering initiation in spring and summer, the growth of expanded flower buds increased significantly, and their shape was obviously enlarged, which indicated that flowering was initiated. A total of 168,120 expressed genes were identified in spring and summer dormant and expanded flower buds, of which 11,687 genes showed significantly differential expression between spring and summer dormant and expanded flower buds. These differentially expressed genes (DEGs) were mainly involved in plant hormone signal transduction, metabolic processes, cellular components, binding, and catalytic activity. Analysis of differential gene expression patterns revealed that gibberellin signaling, and some transcription factors were closely involved in the regulation of spring and summer flowering initiation in ‘Changchun’. A qRT-PCR (quantitative Real Time Polymerase Chain Reaction) analysis showed that BGISEQ-500 sequencing platform could truly reflect gene expression patterns. It also verified that GID1B (GIBBERELLIN INSENSITIVE DWARF1 B), GID1C, SPL8 (SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 8), and GASA (GIBBERELLIC ACID-STIMULATED ARABIDOPSIS) family genes were expressed at high levels, while the expression of SPY (SPINDLY) was low during spring and summer flowering initiation. Meanwhile, the up- and down-regulated expression of, respectively, AGL6 (AGAMOUS-LIKE 6) and DREB3 (DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEIN 3), AG15, and CDF1 (CYCLIC DOF FACTOR 1) might also be involved in the specific regulation of spring and summer flowering initiation. Obviously, flowering initiation is an important stage of the flowering process in woody plants, involving the specific regulation of relevant genes and transcription factors. This study provides a new perspective for the regulation of the flowering process in perennial woody plants.
Article
Full-text available
miR319 was the first plant miRNA discovered via forward genetic mutation screening. In this study, we found that miR319 family members had similar sequences but different expression patterns in Brassica campestris and Arabidopsis thaliana. RT-PCR analysis revealed that Bra-MIR319a and Bra-MIR319c had similar expression patterns and were widely expressed in plant development, whereas Bra-MIR319b could only be detected in stems. The overexpression of each Bra-MIR319 family member in Arabidopsis could inhibit cell division and function in leaf and petal morphogenesis. Bra-miR319a formed a new regulatory relationship after whole genome triplication, and Bra-MIR319a overexpressing in Arabidopsis led to the degradation of pollen content and affected the formation of intine, thereby causing pollen abortion. Our results suggest that Bra-MIR319 family members have functional similarity and difference in plant development.
Article
Lagerstroemia indica (crape myrtle) is a popular Chinese landscape plant with a long flowering period that contributes to its gorgeous flowers and high ornamental value, which motivate L. indica breeding. We found a wild acarpous individual of L. indica that did not bear seeds after flowering and had a significantly longer flowering period than fructiferous L. indica . This study identified differences in floral organ morphology, and stamen and pistil structure between fructiferous and acarpous L. indica through observation, paraffin sectioning, and scanning electron microscopy (SEM). The flowering time of each acarpous L. indica inflorescence lasts as long as 18 to 25 days. When a single flower withers, it falls from the pedicel without any fruit. The abortion in the floral organ of acarpous L. indica is characterized by sterile and undehisced anthers, pollen abortion, and deformed and irregularly arranged filament cells. Acarpous L. indica features short and loosely arranged papilla cells in the stigma, a flat style and narrow stylar canal, loosely arranged epidermal cells, and no obvious nuclei. No embryo sac cavity is found in acarpous L. indica ovules. In some nucelli, the egg apparatus structure can be observed indistinctly but without cell contour. In others, the egg apparatus structure is completely absent, and only flocculent tissue is observed. This study may provide a theoretical foundation for future studies on the molecular mechanisms of the mutations in acarpous L. indica .
Article
As one of the most popular woody species that blooms in summer, Lagerstroemia speciosa has been used abundantly in urban landscape for its excellent floral beauty. For the first time, we discovered a double-flower variant with all petaloid stamens. To understand the molecular basis of this variation, we contrasted the transcriptomes of single- and double-flower buds at three stamen development stages. In total, 73,536 unigenes were mapped and 30,714 differently expressed genes (DEGs) were identified in the tissues. We focused on the DEGs expressing in both phenotypes and investigated the association of their expression profiles with their functions in transcription pathways. Furthermore, we performed WGCNA and identified co-expressed genes with four floral homeotic genes as hubs (MADS16, Unigene0026169; AP2, Unigene0042732; SOC1, Unigene0046314; AG, Unigene0056437). The expression of these hub genes has been conserved across the three developmental stages but significantly different between the two floral phenotypes. As a result, the robust transcriptional regulation of stamen petaloidy in double flowers was deduced. These findings will help to unravel the regulatory mechanisms of several specific genes, thereby providing a basis to study double-flower molecular breeding in L. speciosa.
Article
This review focuses on the current knowledge of transcription factors involved in Arabidopsis anther development. Anther development is a multistage process and controlled by a complex network of transcription factors acting in spatio/temporal manner. Molecular understanding of anther developmental pathway is critical from the perspective of controlling male fertility and hybrid generation. Generation of hybrid lines relies upon the effective mechanisms of controlling the process of pollen development and pollen release. Controlling any developmental program requires a good knowledge of regulatory pathways governing that developmental program. In a regulatory pathway, transcription factors represent an important link between the developmental program and response of genes to growth regulators and environmental signals. Therefore, identifying the entire cohort of anther specific transcription factors is an essential step towards the molecular understanding of regulatory networks involved in pollen formation and pollen release.