Seed development

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    Arabidopsis BIG1 and BIG5 are crucial for male gametophyte transmission
    Yiping Suo and Jirong Huang
    J Integr Plant Biol 2019, 61 (9): 981-986.  
    doi: 10.1111/jipb.12731
    Abstract (Browse 325)  |   Save

    Arabidopsis contains five Brefeldin A‐inhibited guanine nucleotide exchange factors (BIGs), which play a critical role in vesicle biogenesis for protein traffic from the Golgi to the plasma membrane. Biological processes regulated by BIG1‐BIG4 are postulated to be distinct from those by BIG5. However, we show that the self‐pollinated BIG1+/− big5 silique do not produce homozygous seeds, and some pollen tubes from BIG1+/− big5 anthers grew slowly in vitro and failed to target nearby ovules in vivo. We identified the big1 big5 homozygote from the progeny of BIG1+/− big5 plants transformed with BIG5, whose expression is driven by a pollen‐specific promoter pLat52, indicating that male gametophyte transmission is blocked in the double mutant. Confocal microscopy indicated that BIG1 and BIG5 are co‐localized in trans Golgi network. Thus, our data indicate that BIG1 and BIG5 are crucial for male gametophyte transmission.

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    Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata)
    Yi-Can Zhang, Ying-Ning Zou, Li-Ping Liu and Qiang-Sheng Wu
    J Integr Plant Biol 2019, 61 (10): 1099-1111.  
    DOI: 10.1111/jipb.12743
    Abstract (Browse 235)  |   Save
    Citrus canker, caused by Xanthomonas axonopodis pv. citri (‘Xac’), is an important quarantine disease in citrus crops. Arbuscular mycorrhizal fungi (AMF) form symbiotic interactions with host plants and further affect their disease resistance, possibly by modulating the activity of salicylic acid (SA), a key phytohormone in disease resistance. Common mycorrhizal networks (CMNs) can interconnect plants, but it is not yet clear whether CMNs promote resistance to citrus canker and, if so, whether SA signaling is involved in this process. To test this possibility, we used a two‐chambered rootbox to establish CMNs between trifoliate orange (Poncirus trifoliata) seedlings in chambers inoculated (treated) or not (neighboring) with the AMF, Paraglomus occultum. A subset of the AMF‐inoculated seedlings were also inoculated with Xac (+AMF+Xac). At 2 d post‐inoculation (dpi), compared with the +AMF−Xac treatment, neighboring seedlings in +AMF+Xac treatment had lower expression levels of the SA biosynthetic genes, PtPAL, PtEPS1, and PtPBS3, but higher SA levels, which attributed to the upregulation of PtPAL and PtPBS3 in treated seedlings and the transfer of SA, via CMNs, to the neighboring seedlings. At 4 dpi, the pathogenesis‐related (PR) protein genes, PtPR1, PtPR4, and PtPR5, and the transcriptional regulatory factor gene, PtNPR1, were activated in neighboring seedlings of +AMF+Xac treatment. At 9 dpi, root phenylalanine ammonia‐lyase activity and total soluble phenol and lignin concentrations increased in neighboring seedlings of +AMF+Xac treatment, likely due to the linkage and signal transfer, via CMNs. These findings support the hypothesis that CMNs transfer the SA signal from infected to neighboring healthy seedlings, to activate defense responses and affording protection to neighboring plants against citrus canker infection.
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    A VPE-like protease NtTPE8 exclusively expresses in the integumentary tapetum and is involved in seed development
    Wei Wang, Hanxian Xiong, Rongxin Lin, Nantian Zhao, Peng Zhao and Meng-Xiang Sun
    J Integr Plant Biol 2019, 61 (5): 598-610.  
    doi: 10.1111/jipb.12766
    Abstract (Browse 335)  |   Save
    Programmed cell death (PCD) is an essential process for development, and shows conserved cytological features in both plants and animals. Caspases are well-known critical components of the PCD machinery in animals. However, currently few typical counterparts have been identified in plants and only several caspase-like proteases are known to be involved in plant PCD, indicating the existence of great challenge for confirming new caspase-like proteases and elucidating the mechanisms regulating plant PCD. Here, we report a novel cysteine protease, NtTPE8, which was extracted from tobacco seeds and confirmed as a new caspase-like protease. Recombinant NtTPE8 exhibited legumain and caspase-like proteolytic activities, both of which could be inhibited by the pan-caspase inhibitor (Z-VAD-FMK). Notably, NtTPE8 possessed several caspase activities and the capacity to cleave the cathepsin H substrate FVR, indicating a unique character of NtTPE8. NtTPE8 was exclusively expressed in the integumentary tapetum and thus, is the first specific molecular marker reported to date for this cell type. Down-regulation of NtTPE8 caused seed abortion, via disturbing early embryogenesis, indicating its critical role in embryogenesis and seed development. In conclusion, we identified a novel caspase-like cysteine protease, NtTPE8, exclusively expressed in the integumentary tapetum that is involved in seed development.
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    Seed germination and dormancy: The classic story, new puzzles, and evolution
    Hiroyuki Nonogaki
    J Integr Plant Biol 2019, 61 (5): 541-563.  
    doi: 10.1111/jipb.12762
    Abstract (Browse 412)  |   Save
    This review highlights recent progresses in seed germination and dormancy research. Research on the weakening of the endosperm during germination, which is almost a classic theme in seed biology, was resumed by α-xylosidase studies. Strong genetic evidence was presented to suggest that the quality control of xyloglucan biosynthesis in the endosperm (and the embryo) plays a critical role in germination. Further analyses on the endosperm and the adjacent layers have suggested that the cutin coat in the endosperm-testa interphase negatively affects germination while the endosperm-embryo interphase produces a sheath that facilitates germination. These progresses significantly advanced our understanding of seed germination mechanisms. A breakthrough in dormancy research, on the other hand, revealed the unique abscisic acid signaling pathway that is regulated by DELAY OF GERMINATION1 (DOG1). The detailed analysis of DOG1 expression uncovered the intriguing story of reciprocal regulation of the sense-antisense pair, which generated new questions. Recent studies also suggested that the DOG1 function is not limited to dormancy but extended through general seed maturation, which provokes questions about the evolution of DOG1 family proteins. Seed biology is becoming more exciting with the classic stories being revitalized and new puzzles emerging from the frontier.
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    Peroxisomes in plant reproduction and seed-related development
    Ronghui Pan, Jun Liu and Jianping Hu
    J Integr Plant Biol 2019, 61 (7): 784-802.  
    doi: 10.1111/jipb.12765
    Abstract (Browse 256)  |   Save
    Peroxisomes are small multi-functional organelles essential for plant development and growth. Plant peroxisomes play various physiological roles, including phytohormone biosynthesis, lipid catabolism, reactive oxygen species metabolism and many others. Mutant analysis demonstrated key roles for peroxisomes in plant reproduction, seed development and germination and post-germinative seedling establishment; however, the underlying mechanisms remain to be fully elucidated. This review summarizes findings that reveal the importance and complexity of the role of peroxisomes in the pertinent processes. The β-oxidation pathway plays a central role, whereas other peroxisomal pathways are also involved. Understanding the biochemical and molecular mechanisms of these peroxisomal functions will be instrumental to the improvement of crop plants.
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    A strategy for generating rice apomixis by gene editing
    En Xie, Yafei Li, Ding Tang, Yanli Lv, Yi Shen and Zhukuan Cheng
    J Integr Plant Biol 2019, 61 (8): 911-916.  
    doi: 10.1111/jipb.12785
    Abstract (Browse 507)  |   Save

    Apomixis is an asexual reproduction way of plants that can produce clonal offspring through seeds. In this study, we introduced apomixis into rice (Oryza sativa) by mutating OsSPO11‐1, OsREC8, OsOSD1, and OsMATL through a CRISPR/Cas9 system. The quadruple mutant showed a transformation from meiosis to mitosis and produced clonal diploid gametes. With mutated Osmatl, which gives rise to haploid induction in plants, the quadruple mutant is expected to be able to be produced apomictic diploid offspring. We named this quadruple mutant as AOP (Apomictic Offspring Producer) for its ability to produce apomictic offspring.

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    PEX16 contributions to peroxisome import and metabolism revealed by viable Arabidopsis pex16 mutants
    Sarah E. Burkhart, Roxanna J. Llinas and Bonnie Bartel
    J Integr Plant Biol 2019, 61 (7): 853-870.  
    doi: 10.1111/jipb.12789
    Abstract (Browse 206)  |   Save
    Peroxisomes rely on peroxins (PEX proteins) for biogenesis, importing membrane and matrix proteins, and fission. PEX16, which is implicated in peroxisomal membrane protein targeting and forming nascent peroxisomes from the endoplasmic reticulum (ER), is unusual among peroxins because it is inserted co-translationally into the ER and localizes to both ER and peroxisomal membranes. PEX16 mutations in humans, yeast, and plants confer some common peroxisomal defects; however, apparent functional differences have impeded the development of a unified model for PEX16 action. The only reported pex16 mutant in plants, the Arabidopsis shrunken seed1 mutant, is inviable, complicating analysis of PEX16 function after embryogenesis. Here, we characterized two viable Arabidopsis pex16 alleles that accumulate negligible PEX16 protein levels. Both mutants displayed impaired peroxisome function - slowed consumption of stored oil bodies, decreased import of matrix proteins, and increased peroxisome size. Moreover, one pex16 allele exhibited reduced growth that could be alleviated by an external fixed carbon source, decreased responsiveness to peroxisomally processed hormone precursors, and worsened or improved peroxisome function in combination with other pex mutants. Because the mutations impact different regions of the PEX16 gene, these viable pex16 alleles allow assessment of the importance of Arabidopsis PEX16 and its functional domains.
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    New guidelines for fluorophore application in peroxisome targeting analyses in transient plant expression systems
    Christian Falter, Nguyen Binh Anh Thu, Saugat Pokhrel and Sigrun Reumann
    J Integr Plant Biol 2019, 61 (7): 884-899.  
    doi: 10.1111/jipb.12791
    Abstract (Browse 230)  |   Save
    Peroxisome research has been revolutionized by proteome studies combined with in vivo subcellular targeting analyses. Yellow and cyan fluorescent protein (YFP and CFP) are the classical fluorophores of plant peroxisome research. In the new transient expression system of Arabidopsis seedlings co-cultivated with Agrobacterium we detected the YFP fusion of one candidate protein in peroxisomes, but only upon co-transformation with the peroxisome marker, CFP-PTS1. The data suggested that the YFP fusion was directed to peroxisomes due to its weak heterodimerization ability with CFP-PTS1, allowing piggy-back import into peroxisomes. Indeed, if co-expressed with monomeric Cerulean-PTS1 (mCer-PTS1), the YFP fusion was no longer matrix localized. We systematically investigated the occurrence and extent of dimerization-based piggy-back import for different fluorophore combinations in five major transient plant expression systems. In Arabidopsis seedlings and tobacco leaves both untagged YFP and monomeric Venus were imported into peroxisomes if co-expressed with CFP-PTS1 but not with mCer-PTS1. By contrast, piggy-back import of cytosolic proteins was not observed in Arabidopsis and tobacco protoplasts or in onion epidermal cells for any fluorophore combination at any time point. Based on these important results we formulate new guidelines for fluorophore usage and experimental design to guarantee reliable identification of novel plant peroxisomal proteins.
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    Central role of the LEAFY COTYLEDON1 transcription factor in seed development
    Leonardo Jo, Julie M. Pelletier and John J. Harada
    J Integr Plant Biol 2019, 61 (5): 564-580.  
    doi: 10.1111/jipb.12806
    Abstract (Browse 354)  |   Save
    Seed development is a complex period of the flowering plant life cycle. After fertilization, the three main regions of the seed, embryo, endosperm and seed coat, undergo a series of developmental processes that result in the production of a mature seed that is developmentally arrested, desiccated, and metabolically quiescent. These processes are highly coordinated, both temporally and spatially, to ensure the proper growth and development of the seed. The transcription factor, LEAFY COTYLEDON1 (LEC1), is a central regulator that controls several aspects of embryo and endosperm development, including embryo morphogenesis, photosynthesis, and storage reserve accumulation. Thus, LEC1 regulates distinct sets of genes at different stages of seed development. Despite its critical importance for seed development, an understanding of the mechanisms underlying LEC1's multifunctionality is only beginning to be obtained. Recent studies describe the roles of specific transcription factors and the hormones, gibberellic acid and abscisic acid, in controlling the activity and transcriptional specificity of LEC1 across seed development. Moreover, studies indicate that LEC1 acts as a pioneer transcription factor to promote epigenetic reprogramming during embryogenesis. In this review, we discuss the mechanisms that enable LEC1 to serve as a central regulator of seed development.
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    Seed biology
    John Harada
    J Integr Plant Biol 2019, 61 (5): 530-532.  
    doi: 10.1111/jipb.12808
    Abstract (Browse 356)  |   Save
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    Transcriptome landscape of the early Brassica napus seed
    Dylan J. Ziegler, Deirdre Khan, Jenna L. Kalichuk, Michael G. Becker and Mark F. Belmonte
    J Integr Plant Biol 2019, 61 (5): 639-650.  
    doi: 10.1111/jipb.12812
    Abstract (Browse 355)  |   Save
    Brassica napus L. (canola) is one of the world's most economically important oilseeds. Despite our growing knowledge of Brassica genetics, we still know little about the genes and gene regulatory networks underlying early seed development. In this work, we use laser microdissection coupled with RNA sequencing to profile gene activity of both the maternal and filial subregions of the globular seed. We find subregions of the chalazal end including the chalazal endosperm, chalazal proliferating tissue, and chalazal seed coat, have unique transcriptome profiles associated with hormone biosynthesis and polysaccharide metabolism. We confirm that the chalazal seed coat is uniquely enriched for sucrose biosynthesis and transport, and that the chalazal endosperm may function as an important regulator of the maternal region through brassinosteroid synthesis. The chalazal proliferating tissue, a poorly understood subregion, was specifically enriched in transcripts associated with megasporogenesis and trehalose biosynthesis, suggesting this ephemeral structure plays an important role in both sporophytic development and carbon nutrient balance, respectively. Finally, compartmentalization of transcription factors and their regulatory circuits has uncovered previously unknown roles for the chalazal pole in early seed development.
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    OsbZIP76 interacts with OsNF‐YBs and regulates endosperm cellularization in rice (Oryza sativa)
    Baixiao Niu, Hui Deng, Tingting Li, Sandeep Sharma, Qianbin Yun, Qianru Li, Zhiguo E and Chen Chen
    J Integr Plant Biol 2020, 62 (12): 1983-1996.  
    DOI: 10.1111/jipb.12989
    Abstract (Browse 350)  |   Save
    Following double fertilization, plant endosperm nuclei undergo syncytial divisions, followed by synchronous cellularization. Cellularization is a key event during endosperm development, but our understanding of its regulation is limited to Arabidopsis. In this study we show that OsbZIP76 regulates cellularization in rice (Oryza sativa). Activation of OsbZIP76 coincided with the initiation of cellularization, and its knockdown or knockout mutants exhibited precocious cellularization. Genes involved in endosperm development or starch biosynthesis were prematurely activated in the osbzip76 caryopsis. As a putative transcription factor, OsbZIP76 alone lacked transcriptional activation activity; however, it interacted with the nuclear factor Y (NF‐Y) family transcription factors OsNF‐YB9 and OsNF‐YB1 in yeast and in planta. OsbZIP76 and OsNF‐YB9 were predominantly expressed in the endosperm and the proteins colocalized. Seeds of osnf‐yb1 and osbzip76 mutants showed reduced size and reduced apparent amylose content. The parent‐of‐origin‐dependent expression of OsbZIP76 is variable in different rice accessions. In summary, OsbZIP76 is an endosperm‐expressed imprinted gene that regulates endosperm development in rice.
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    N4‐methylcytidine ribosomal RNA methylation in chloroplasts is crucial for chloroplast function, development, and abscisic acid response in Arabidopsis
    Le Nguyen Tieu Ngoc, Su Jung Park, Trinh Thi Huong, Kwang Ho Lee and Hunseung Kang
    J Integr Plant Biol 2021, 63 (3): 570-582.  
    doi: 10.1111/jipb.13009
    Abstract (Browse 316)  |   Save
    Although the essential role of messenger RNA methylation in the nucleus is increasingly understood, the nature of ribosomal RNA (rRNA) methyltransferases and the role of rRNA methylation in chloroplasts remain largely unknown. A recent study revealed that CMAL (for Chloroplast mr aW‐ Like) is a chloroplast‐localized rRNA methyltransferase that is responsible for N4‐methylcytidine (m4C) in 16S chloroplast rRNA in Arabidopsis thaliana. In this study, we further examined the role of CMAL in chloroplast biogenesis and function, development, and hormone response. The cmal mutant showed reduced chlorophyll biosynthesis, photosynthetic activity, and growth‐defect phenotypes, including severely stunted stems, fewer siliques, and lower seed yield. The cmal mutant was hypersensitive to chloroplast translation inhibitors, such as lincomycin and erythromycin, indicating that the m4C‐methylation defect in the 16S rRNA leads to a reduced translational activity in chloroplasts. Importantly, the stunted stem of the cmal mutant was partially rescued by exogenous gibberellic acid or auxin. The cmal mutant grew poorer than wild type, whereas the CMAL‐overexpressing transgenic Arabidopsis plants grew better than wild type in the presence of abscisic acid. Altogether, these results indicate that CMAL is an indispensable rRNA methyltransferase in chloroplasts and is crucial for chloroplast biogenesis and function, photosynthesis, and hormone response during plant growth and development.
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    A rare Waxy allele coordinately improves rice eating and cooking quality and grain transparency
    Changquan Zhang, Yong Yang, Shengjie Chen, Xueju Liu, Jihui Zhu, Lihui Zhou, Yan Lu, Qianfeng Li, Xiaolei Fan, Shuzhu Tang, Minghong Gu and Qiaoquan Liu
    J Integr Plant Biol 2021, 63 (5): 889-901.  
    doi: 10.1111/jipb.13010
    Abstract (Browse 487)  |   Save
    In rice (Oryza sativa), amylose content (AC) is the major factor that determines eating and cooking quality (ECQ). The diversity in AC is largely attributed to natural allelic variation at the Waxy (Wx) locus. Here we identified a rare Wx allele, Wxmw, which combines a favorable AC, improved ECQ and grain transparency. Based on a phylogenetic analysis of Wx genomic sequences from 370 rice accessions, we speculated that Wxmw may have derived from recombination between two important natural Wx alleles, Wxin and Wxb. We validated the effects of Wxmw on rice grain quality using both transgenic lines and near‐isogenic lines (NILs). When introgressed into the japonica Nipponbare (NIP) background, Wxmw resulted in a moderate AC that was intermediate between that of NILs carrying the Wxb allele and NILs with the Wxmp allele. Notably, mature grains of NILs fixed for Wxmw had an improved transparent endosperm relative to soft rice. Further, we introduced Wxmw into a high‐yielding japonica cultivar via molecular marker‐assisted selection: the introgressed lines exhibited clear improvements in ECQ and endosperm transparency. Our results suggest that Wxmw is a promising allele to improve grain quality, especially ECQ and grain transparency of high‐yielding japonica cultivars, in rice breeding programs.
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    The origin of Wxla provides new insights into the improvement of grain quality in rice
    Hao Zhou, Duo Xia, Da Zhao, Yanhua Li, Pingbo Li, Bian Wu, Guanjun Gao, Qinglu Zhang, Gongwei Wang, Jinghua Xiao, Xianghua Li, Sibin Yu, Xingming Lian and Yuqing He
    J Integr Plant Biol 2021, 63 (5): 878-888.  
    doi: 10.1111/jipb.13011
    Abstract (Browse 468)  |   Save
    Appearance and taste are important factors in rice (Oryza sativa) grain quality. Here, we investigated the taste scores and related eating‐quality traits of 533 diverse cultivars to assess the relationships between—and genetic basis of—rice taste and eating‐quality. A genome‐wide association study highlighted the Wx gene as the major factor underlying variation in taste and eating quality. Notably, a novel waxy (Wx) allele, Wxla, which combined two mutations from Wxb and Wxin, exhibited a unique phenotype. Reduced GBSSI activity conferred Wxla rice with both a transparent appearance and good eating quality. Haplotype analysis revealed that Wxla was derived from intragenic recombination. In fact, the recombination rate at the Wx locus was estimated to be 3.34 kb/cM, which was about 75‐fold higher than the genome‐wide mean, indicating that intragenic recombination is a major force driving diversity at the Wx locus. Based on our results, we propose a new network for Wx evolution, noting that new Wx alleles could easily be generated by crossing genotypes with different Wx alleles. This study thus provides insights into the evolution of the Wx locus and facilitates molecular breeding for quality in rice.
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    Enhanced production of seed oil with improved fatty acid composition by overexpressing NAD+-dependent glycerol-3-phosphate dehydrogenase in soybean
    Ying Zhao, Pan Cao, Yifan Cui, Dongxu Liu, Jiapeng Li, Yabin Zhao, Siqi Yang, Bo Zhang, Runnan Zhou, Minghao Sun, Xuetian Guo, Mingliang Yang, Dawei Xin, Zhanguo Zhang, Xin Li, Chen Lv, Chunyan Liu, Zhaoming Qi, Jingyu Xu, Xiaoxia Wu and Qingshan Chen
    J Integr Plant Biol 2021, 63 (6): 1036-1053.  
    doi: 10.1111/jipb.13094
    Abstract (Browse 336)  |   Save
    There is growing interest in expanding the production of soybean oils (mainly triacylglycerol, or TAG) to meet rising feed demand and address global energy concerns. We report that a plastid-localized glycerol-3-phosphate dehydrogenase (GPDH), encoded by GmGPDHp1 gene, catalyzes the formation of glycerol-3-phosphate (G3P), an obligate substrate required for TAG biosynthesis. Overexpression of GmGPDHp1 increases soybean seed oil content with high levels of unsaturated fatty acids (FAs), especially oleic acid (C18:1), without detectably affecting growth or seed protein content or seed weight. Based on the lipidomic analyses, we found that the increase in G3P content led to an elevated diacylglycerol (DAG) pool, in which the Kennedy pathway-derived DAG was mostly increased, followed by PC-derived DAG, thereby promoting the synthesis of TAG containing relatively high proportion of C18:1. The increased G3P levels induced several transcriptional alterations of genes involved in the glycerolipid pathways. In particular, genes encoding the enzymes responsible for de novo glycerolipid synthesis were largely upregulated in the transgenic lines, in-line with the identified biochemical phenotype. These results reveal a key role for GmGPDHp1-mediated G3P metabolism in enhancing TAG synthesis and demonstrate a strategy to modify the FA compositions of soybean oils for improved nutrition and biofuel.
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