Special Issue: Sexual plant reproduction   

September 2017, Volume 59 Issue 9, Pages 589每707.


Cover Caption: Sexual plant reproduction
The cover shows the RFP protein synthesis in the synergid cell of a SNAIL1-GFP labeled ovule. The synchrony of female gametophyte development is essential for successful male-female communication and sexual reproduction. In this issue, Hao et al. (629每641) report that a nucleolar-localized protein SNAIL1 involved in ribosome biogenesis is required for synchronous development of female gametophyte in Arabidopsis.

 

          Editorial
Plant reproduction: Recent discoveries from China  
Author: Li-Jia Qu and Meng-Xiang Sun
Journal of Integrative Plant Biology 2017 59(9): 591每593
Published Online: August 14, 2017
DOI: 10.1111/jipb.12576
Abstract (Browse 34)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
          Letters to the Editor
Arabidopsis adaptor protein 1G is critical for pollen development  
Author: Chong Feng, Jia-Gang Wang, Hai-Hong Liu, Sha Li and Yan Zhang
Journal of Integrative Plant Biology 2017 59(9): 594每599
Published Online: May 24, 2017
DOI: 10.1111/jipb.12556
      
    

Pollen development is a pre-requisite for sexual reproduction of angiosperms, during which various cellular activities are involved. Pollen development accompanies dynamic remodeling of vacuoles through fission and fusion, disruption of which often compromises pollen viability. We previously reported that the Y subunit of adaptor protein 1 (AP1G) mediates synergid degeneration during pollen tube reception. Here, we demonstrate that AP1G is essential for pollen development. AP1G loss-of-function resulted in male gametophytic lethality due to defective pollen development. By ultrastructural analysis and fluorescence labeling, we demonstrate that AP1G loss-of-function compromised dynamic vacuolar remodeling during pollen development and impaired vacuolar acidification of pollen. Results presented here support a key role of vacuoles in gametophytic pollen development.

Abstract (Browse 187)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
AP1G, adaptor protein 1, is essential for protein sorting at the trans-Golgi network/early endosomes. This study demonstrates that functional loss of the 污 subunit of AP1G resulted in male gametophytic lethality by affecting vacuolar remodeling and acidification during pollen development.
The signals to trigger the initiation of ovule enlargement are from the pollen tubes: The direct evidence  
Author: Sheng Zhong, Jun Zhang and Li-Jia Qu
Journal of Integrative Plant Biology 2017 59(9): 600每603
Published Online: August 16, 2017
DOI: 10.1111/jipb.12577
      
    

In angiosperms, initiation of ovule enlargement represents the start of seed development, the molecular mechanism of which is not yet elucidated. It was previously reported that pollen tube contents, rather than double fertilization, can trigger ovule enlargement. However, it remains unclear whether the signal(s) to trigger the initiation of ovule enlargement are from the sperm cells or from the pollen tubes. Recently, we identified a mutant drop1− drop2−, which produces pollen tubes with no sperm cells. Taking advantage of this special genetic material, we conducted pollination assays, and found that the ovules pollinated with drop1− drop2− pollen could initiate the enlargement and exhibited significant enlarged sizes at 36 h after pollination in comparison with those unpollinated ovules. However, the sizes of the ovules pollinated with drop1− drop2− pollen are significantly smaller than those of the ovules pollinated with wild-type pollen. These results demonstrate that the pollen tube, rather than the sperm cells, release the signal to trigger the initiation of ovule enlargement, and that double fertilization is required for further enlargement of the seeds.

Abstract (Browse 30)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Seed size is an important trait of higher plants, especially of crops that are food resources for humans. Ovule enlargement is the start of seed size expansion. We find that the signal to trigger ovule enlargement comes from the pollen tube, not from the sperm cells, or from fertilization.
          Research Articles
Arabidopsis shaker pollen inward K+ channel SPIK functions in SnRK1 complex-regulated pollen hydration on the stigma  
Author: Dan-Dan Li, Huan Guan, Fei Li, Chang-Zhen Liu, Yu-Xiu Dong, Xian-Sheng Zhang and Xin-Qi Gao
Journal of Integrative Plant Biology 2017 59(9): 604每611
Published Online: June 21, 2017
DOI: 10.1111/jipb.12563
      
    

Pollen hydration is a critical step that determines pollen germination on the stigma. KINβγ is a plant-specific subunit of the SNF1-related protein kinase 1 complex (SnRK1 complex). In pollen of the Arabidopsis kinβγ mutant, the levels of reactive oxygen species were decreased which lead to compromised hydration of the mutant pollen on the stigma. In this study, we analyzed gene expression in kinβγ mutant pollen by RNA-seq and found the expression of inward shaker K+ channel SPIK was down-regulated in the kinβγ pollen. Furthermore, we showed that the pollen hydration of the Arabidopsis spik mutant was defective on the wild-type stigma, although the mutant pollen demonstrated normal hydration in vitro. Additionally, the defective hydration of spik mutant pollen could not be rescued by the wild-type pollen on the stigma, indicating that the spik mutation deprived the capability of pollen absorption on the stigma. Our results suggest that the Arabidopsis SnRK1 complex regulates SPIK expression, which functions in determining pollen hydration on the stigma.

Abstract (Browse 74)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Pollen hydration is a critical step that determines pollen germination on the stigma. In this study, we found that Arabidopsis SnRK1 complex regulates the expression of SPIK, a plasma membrane-localized K+ channel, which functions in mediating pollen hydration on the surface of the stigma.
The polyketide synthase OsPKS2 is essential for pollen exine and Ubisch body patterning in rice  
Author: Xiaolei Zhu, Jing Yu, Jianxin Shi, Takayuki Tohge, Alisdair R. Fernie, Sagit Meir, Asaph Aharoni, Dawei Xu, Dabing Zhang and Wanqi Liang
Journal of Integrative Plant Biology 2017 59(9): 612每628
Published Online: August 7, 2017
DOI: 10.1111/jipb.12574
      
    

Lipid and phenolic metabolism are important for pollen exine formation. In Arabidopsis, polyketide synthases (PKSs) are essential for both sporopollenin biosynthesis and exine formation. Here, we characterized the role of a polyketide synthase (OsPKS2) in male reproduction of rice (Oryza sativa). Recombinant OsPKS2 catalyzed the condensation of fatty acyl-CoA with malonyl-CoA to generate triketide and tetraketide α-pyrones, the main components of pollen exine. Indeed, the ospks2 mutant had defective exine patterning and was male sterile. However, the mutant showed no significant reduction in sporopollenin accumulation. Compared with the WT (wild type), ospks2 displayed unconfined and amorphous tectum and nexine layers in the exine, and less organized Ubisch bodies. Like the pksb/lap5 mutant of the Arabidopsis ortholog, ospks2 showed broad alterations in the profiles of anther-related phenolic compounds. However, unlike pksb/lap5, in which most detected phenolics were substantially decreased, ospks2 accumulated higher levels of phenolics. Based on these results and our observation that OsPKS2 is unable to fully restore the exine defects in the pksb/lap5, we propose that PKS proteins have functionally diversified during evolution. Collectively, our results suggest that PKSs represent a conserved and diversified biochemical pathway for anther and pollen development in higher plants.

Abstract (Browse 36)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The pollen exine is sculptured in a genetically determined manner, but the mechanism controlling exine pattern formation remains unclear. This study demonstrated that a rice polyketide synthase OsPKS2 plays an important role in exine patterning. Mutation in OsPKS2 leads to dramatic changes in pollen exine morphology but does not significantly affect sporopollenin production.
SNAIL1 is essential for female gametogenesis in Arabidopsis thaliana  
Author: Lihong Hao, Xiaolin Wei, Jiulei Zhu, Jiao Shi, Jingjing Liu, Hongya Gu, Tomohiko Tsuge and Li-Jia Qu
Journal of Integrative Plant Biology 2017 59(9): 629每641
Published Online: August 4, 2017
DOI: 10.1111/jipb.12572
      
    

Two yeast Brix family members Ssf1 and Ssf2, involved in large ribosomal subunit synthesis, are essential for yeast cell viability and mating efficiency. Their putative homologs exist in the Arabidopsis genome; however, their role in plant development is unknown. Here, we show that Arabidopsis thaliana SNAIL1 (AtSNAIL1), a protein sharing high sequence identity with yeast Ssf1 and Ssf2, is critical to mitosis progression of female gametophyte development. The snail1 homozygous mutant was nonviable and its heterozygous mutant was semi-sterile with shorter siliques. The mutation in SNAIL1 led to absence of female transmission and reduced male transmission. Further phenotypic analysis showed that the synchronic development of female gametophyte in the snail1 heterozygous mutant was greatly impaired and the snail1 pollen tube growth, in vivo, was also compromised. Furthermore, SNAIL1 was a nucleolar-localized protein with a putative role in protein synthesis. Our data suggest that SNAIL1 may function in ribosome biogenesis like Ssf1 and Ssf2 and plays an important role during megagametogenesis in Arabidopsis.

Abstract (Browse 35)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The coordinated development of female gametophytes is important for plant sexual reproduction. Yeast proteins Ssf1 and Ssf2, involved in ribosome biogenesis, are essential for yeast cell viability. Here we characterized SNAIL1, the Arabidopsis counterpart of them, is required for the synchronous development during female gametogenesis by affecting protein synthesis.
Acetylglutamate kinase is required for both gametophyte function and embryo development in Arabidopsis thaliana  
Author: Jie Huang, Dan Chen, Hailong Yan, Fei Xie, Ying Yu, Liyao Zhang, Mengxiang Sun and Xiongbo Peng
Journal of Integrative Plant Biology 2017 59(9): 642每656
Published Online: March 15, 2017
DOI: 10.1111/jipb.12536
      
    

The specific functions of the genes encoding arginine biosynthesis enzymes in plants are not well characterized. We report the isolation and characterization of Arabidopsis thaliana N-acetylglutamate kinase (NAGK), which catalyzes the second step of arginine biosynthesis. NAGK is a plastid-localized protein and is expressed during most developmental processes in Arabidopsis. Heterologous expression of the Arabidopsis NAGK gene in a NAGK-deficient Escherichia coli strain fully restores bacterial growth on arginine-deficient medium. nagk mutant pollen tubes grow more slowly than wild type pollen tubes and the phenotype is restored by either specifically through complementation by NAGK in pollen, or exogenous supplementation of arginine. nagk female gametophytes are defective in micropylar pollen tube guidance due to the fact that female gametophyte cell fate specification was specifically affected. Expression of NAGK in synergid cells rescues the defect of nagk female gametophytes. Loss-of-function of NAGK results in Arabidopsis embryos not developing beyond the four-celled embryo stage. The embryo-defective phenotype in nagk/NAGK plants cannot be rescued by watering nagk/NAGK plants with arginine or ornithine supplementation. In conclusion, our results reveal a novel role of NAGK and arginine in regulating gametophyte function and embryo development, and provide valuable insights into arginine transport during embryo development.

Abstract (Browse 235)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Arabidopsis thaliana N-acetylglutamate kinase (NAGK) was identified as a functional homolog of Escherichia coli NAGK for catalyzing the second step of arginine biosynthesis. Loss-of-function of NAGK decreased pollen tubes' growth rate, affected female gametophyte cell fate and showed an embryonic lethal phenotype.
A reciprocal inhibition between ARID1 and MET1 in male and female gametes in Arabidopsis  
Author: Lei Li, Wenye Wu, Youshang Zhao and Binglian Zheng
Journal of Integrative Plant Biology 2017 59(9): 657每668
Published Online: August 7, 2017
DOI: 10.1111/jipb.12573
      
    

Both female and male gametophytes harbor companion cells and gametes. MET1, a DNA methyltransferase, is down-regulated in companion cells. However, how MET1 is differentially regulated in gametophytes remains unexplored. ARID1, a transcription factor that is specifically depleted in sperm cells, is occupied by MET1-dependent CG methylation. Here, we show that MET1 confines ARID1 to the vegetative cell of male gametes, but ARID1 conversely represses MET1 in the central cell of female gametes. Compared to the vegetative cell-localization in wild type pollen, ARID1 expands to sperm cells in the met1 mutant. To understand whether MET1-dependent ARID1 inhibition exists during female gametogenesis, we first show that ARID1 is expressed in the megaspore mother cell (MMC), ARID1 but not MET1 is detectable in the central cell at maturity. Interestingly, compared to the absence of MET1 in the central cell and the egg cell of wild type ovules, MET1 significantly accumulates in these two cells in arid1 ovules. Lastly, we show that both ARID1 and MET1 are required for the cell specification of MMC. Collectively, our results uncover a reciprocal dependence between ARID1 and MET1, and provide a clue to further understand how the specification of MMC is likely regulated by DNA methylation.

Abstract (Browse 37)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
DNA methylation is usually down-regulated in companion cells of plant gametes, in which either DNA methytransferases are repressed and/or DNA demethylases are locally increased. This work identified an Arabidopsis transcription factor ARID1 (AT-Rich Interacting Domain 1), which reciprocally regulates MET1, a major CG DNA methyltransferase, during plant gametophyte development.
Suppression or knockout of SaF/SaM overcomes the Sa-mediated hybrid male sterility in rice  
Author: Yongyao Xie, Baixiao Niu, Yunming Long, Gousi Li, Jintao Tang, Yaling Zhang, Ding Ren, Yao-Guang Liu and Letian Chen
Journal of Integrative Plant Biology 2017 59(9): 669每679
Published Online: June 21, 2017
DOI: 10.1111/jipb.12564
      
    

Hybrids between the indica and japonica subspecies of rice (Oryza sativa) are usually sterile, which hinders utilization of heterosis in the inter-subspecific hybrid breeding. The complex locus Sa comprises two adjacently located genes, SaF and SaM, which interact to cause abortion of pollen grains carrying the japonica allele in japonica-indica hybrids. Here we showed that silencing of SaF or SaM by RNA interference restored male fertility in indica-japonica hybrids with heterozygous Sa. We further used clustered regularly interspaced short palindromic repeats (CRISPR)/Cas9-based genome editing to knockout the SaF and SaM alleles, respectively, of an indica rice line to create hybrid-compatible lines. The resultant artificial neutral alleles did not affect pollen viability and other agricultural traits, but did break down the reproductive barrier in the hybrids. We found that some rice lines have natural neutral allele Sa-n, which was compatible with the typical japonica or indica Sa alleles in hybrids. Our results demonstrate that SaF and SaM are required for hybrid male sterility, but are not essential for pollen development. This study provides effective approaches for the generation of hybrid-compatible lines by knocking out the Sa locus or using the natural Sa-n allele to overcome hybrid male sterility in rice breeding. © 2017 The Authors. Bioelectromagnetics published by Wiley Periodicals, Inc.

Abstract (Browse 92)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
Hybrid sterility is a major obstacle to utilization hybrid vigor. Here, we demonstrate effective ways to overcome the Sa-mediated indica-japonica hybrid male sterility in rice by knocking out/down of SaF/SaM genes, or using natural Sa-neutral alleles.
ZYGOTE-ARREST 3 that encodes the tRNA ligase is essential for zygote division in Arabidopsis  
Author: Ke-Jin Yang, Lei Guo, Xiu-Li Hou, Hua-Qin Gong and Chun-Ming Liu
Journal of Integrative Plant Biology 2017 59(9): 680每692
Published Online: June 20, 2017
DOI: 10.1111/jipb.12561
      
    

In sexual organisms, division of the zygote initiates a new life cycle. Although several genes involved in zygote division are known in plants, how the zygote is activated to start embryogenesis has remained elusive. Here, we showed that a mutation in ZYGOTE-ARREST 3 (ZYG3) in Arabidopsis led to a tight zygote-lethal phenotype. Map-based cloning revealed that ZYG3 encodes the transfer RNA (tRNA) ligase AtRNL, which is a single-copy gene in the Arabidopsis genome. Expression analyses showed that AtRNL is expressed throughout zygotic embryogenesis, and in meristematic tissues. Using pAtRNL::cAtRNL-sYFP-complemented zyg3/zyg3 plants, we showed that AtRNL is localized exclusively in the cytoplasm, suggesting that tRNA splicing occurs primarily in the cytoplasm. Analyses using partially rescued embryos showed that mutation in AtRNL compromised splicing of intron-containing tRNA. Mutations of two tRNA endonuclease genes, SEN1 and SEN2, also led to a zygote-lethal phenotype. These results together suggest that tRNA splicing is critical for initiating zygote division in Arabidopsis.

Abstract (Browse 107)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The Arabidopsis zyg3 mutant exhibits a tight zygote-lethal phenotype. ZYG3, expressed in zygote and developing embryos, encodes a tRNA ligase which is essential for the splicing of tRNATyr and elongator tRNAMet, suggesting the critical role of tRNA splicing in the initiation of zygote divisions in plants.
Regulatory network and genetic interactions established by OsMADS34 in rice inflorescence and spikelet morphogenesis  
Author: Qingcai Meng, Xiaofeng Li, Wanwan Zhu, Li Yang, Wanqi Liang, Ludovico Dreni and Dabing Zhang
Journal of Integrative Plant Biology 2017 59(9): 693每707
Published Online: August 26, 2017
DOI: 10.1111/jipb.12594
      
    

Grasses display highly diversified inflorescence architectures that differ in the arrangement of spikelets and flowers and determine cereal yields. However, the molecular basis underlying grass inflorescence morphogenesis remains largely unknown. Here we investigate the role of a functionally diversified SEPALLATA MADS-box transcription factor, OsMADS34, in regulating rice (Oryza sativa L.) inflorescence and spikelet development. Microarray analysis showed that, at the very early stages of inflorescence formation, dysfunction of OsMADS34 caused altered expression of 379 genes that are associated with protein modification and degradation, transcriptional regulation, signaling and metabolism activity. Genetic analysis revealed that OsMADS34 controls different aspects of inflorescence structure, branching and meristem activity synergistically with LAX PANICLE1 (LAX1) and FLORAL ORGAN NUMBER4 (FON4), as evidenced by the enhanced phenotypes of osmads34 lax1 and osmads34 fon4 compared with the single mutants. Additionally, double mutant between osmads34 and the sterile lemma defective mutant elongated empty glume (ele) displayed an enhanced phenotype, that is, longer and wider sterile lemmas that were converted into lemma/palea-like organs, suggesting that ELE and OsMADS34 synergistically control the sterile lemma development. OsMADS34 may act together with OsMADS15 in controlling sterile lemma development. Collectively, these findings provide insights into the regulatory function of OsMADS34 in rice inflorescence and spikelet development.

Abstract (Browse 28)  |  References  |  Full Text HTML  |  Full Text PDF  |  Cited By       
The inflorescence structure is a key determinant of yield in crops. The MADS-box transcription factor OsMADS34 is known to regulate both inflorescence branching and spikelet morphogenesis in rice. Here, we provide new insights into the genetic interactions and the downstream regulatory network established by OsMADS34.
 

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