Seed development

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A recently evolved BAHD acetyltransferase, responsible for bitter soyasaponin A production, is indispensable for soybean seed germination

Jia Yuan, Liya Ma, Yan Wang, Xindan Xu, Rui Zhang, Chengyuan Wang, Wenxiang Meng, Zhixi Tian, Yihua Zhou and Guodong Wang

J Integr Plant Biol 2023, 65 (11): 2490-2504.
DOI: 10.1111/jipb.13553

Abstract (Browse 149) |

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Soyasaponins are major small molecules that accumulate in soybean (Glycine max) seeds. Among them, type-A soyasaponins, fully acetylated at the terminal sugar of their C22 sugar chain, are responsible for the bitter taste of soybean-derived foods. However, the molecular basis for the acetylation of type-A soyasaponins remains unclear. Here, we identify and characterize GmSSAcT1, encoding a BADH-type soyasaponin acetyltransferase that catalyzes three or four consecutive acetylations on type-A soyasaponins in vitro and in planta. Phylogenetic analysis and biochemical assays suggest that GmSSAcT1 likely evolved from acyltransferases present in leguminous plants involved in isoflavonoid acylation. Loss-of-function mutants of GmSSAcT1 exhibited impaired seed germination, which attribute to the excessive accumulation of null-acetylated type-A soyasaponins. We conclude that GmSSAcT1 not only functions as a detoxification gene for high accumulation of type-A soyasaponins in soybean seeds but is also a promising target for breeding new soybean varieties with lower bitter soyasaponin content.

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Cited: Web of Science(1)

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The DEAD-box RNA helicase ZmRH48 is required for the splicing of multiple mitochondrial introns, mitochondrial complex biosynthesis, and seed development in maize

Yan-Zhuo Yang, Shuo Ding, Xin-Yuan Liu, Chunhui Xu, Feng Sun and Bao-Cai Tan

J Integr Plant Biol 2023, 65 (11): 2456-2468.
DOI: 10.1111/jipb.13558

Abstract (Browse 187) |

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RNA helicases participate in nearly all aspects of RNA metabolism by rearranging RNAs or RNA–protein complexes in an adenosine triphosphate-dependent manner. Due to the large RNA helicase families in plants, the precise roles of many RNA helicases in plant physiology and development remain to be clarified. Here, we show that mutations in maize (Zea mays) DEAD-box RNA helicase 48 (ZmRH48) impair the splicing of mitochondrial introns, mitochondrial complex biosynthesis, and seed development. Loss of ZmRH48 function severely arrested embryogenesis and endosperm development, leading to defective kernel formation. ZmRH48 is targeted to mitochondria, where its deficiency dramatically reduced the splicing efficiency of five cis-introns (nad5 intron 1; nad7 introns 1, 2, and 3; and ccmFc intron 1) and one trans-intron (nad2 intron 2), leading to lower levels of mitochondrial complexes I and III. ZmRH48 interacts with two unique pentatricopeptide repeat (PPR) proteins, PPR-SMR1 and SPR2, which are required for the splicing of over half of all mitochondrial introns. PPR-SMR1 interacts with SPR2, and both proteins interact with P-type PPR proteins and Zm-mCSF1 to facilitate intron splicing. These results suggest that ZmRH48 is likely a component of a splicing complex and is critical for mitochondrial complex biosynthesis and seed development.

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A loss-of-function mutant allele of a glycosyl hydrolase gene has been co-opted for seed weight control during soybean domestication

Siming Wei, Bin Yong, Hongwei Jiang, Zhenghong An, Yan Wang, Bingbing Li, Ce Yang, Weiwei Zhu, Qingshan Chen and Chaoying He

J Integr Plant Biol 2023, 65 (11): 2469-2489.
DOI: 10.1111/jipb.13559

Abstract (Browse 200) |

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The resultant DNA from loss-of-function mutation can be recruited in biological evolution and development. Here, we present such a rare and potential case of “to gain by loss” as a neomorphic mutation during soybean domestication for increasing seed weight. Using a population derived from a chromosome segment substitution line of Glycine max (SN14) and Glycine soja (ZYD06), a quantitative trait locus (QTL) of 100-seed weight (qHSW) was mapped on chromosome 11, corresponding to a truncated β-1, 3-glucosidase (βGlu) gene. The novel gene hsw results from a 14-bp deletion, causing a frameshift mutation and a premature stop codon in the βGlu. In contrast to HSW, the hsw completely lost βGlu activity and function but acquired a novel function to promote cell expansion, thus increasing seed weight. Overexpressing hsw instead of HSW produced large soybean seeds, and surprisingly, truncating hsw via gene editing further increased the seed size. We further found that the core 21-aa peptide of hsw and its variants acted as a promoter of seed size. Transcriptomic variation in these transgenic soybean lines substantiated the integration hsw into cell and seed size control. Moreover, the hsw allele underwent selection and expansion during soybean domestication and improvement. Our work cloned a likely domesticated QTL controlling soybean seed weight, revealed a novel genetic variation and mechanism in soybean domestication, and provided new insight into crop domestication and breeding, and plant evolution.

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Is bitter actually better? Targeting a soyasaponin acetyltransferase affects soybean seed germination

Yongshuo Ma and Yi Shang

J Integr Plant Biol 2023, 65 (11): 2409-2411.
DOI: 10.1111/jipb.13563

Abstract (Browse 137) |

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GmJAZ3 interacts with GmRR18a and GmMYC2a to regulate seed traits in soybean

Yang Hu, Yue Liu, Jian‐Jun Tao, Long Lu, Zhi‐Hao Jiang, Jun‐Jie Wei, Chun‐Mei Wu, Cui‐Cui Yin, Wei Li, Ying‐Dong Bi, Yong‐Cai Lai, Wei Wei, Wan‐Ke Zhang, Shou‐Yi Chen and Jin‐Song Zhang

J Integr Plant Biol 2023, 65 (8): 1983-2000.
doi: 10.1111/jipb.13494

Abstract (Browse 436) |

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Seed weight is usually associated with seed size and is one of the important agronomic traits that determine yield. Understanding of seed weight control is limited, especially in soybean plants. Here we show that Glycine max JASMONATE-ZIM DOMAIN 3 (GmJAZ3), a gene identified through gene co-expression network analysis, regulates seed-related traits in soybean. Overexpression of GmJAZ3 promotes seed size/weight and other organ sizes in stable transgenic soybean plants likely by increasing cell proliferation. GmJAZ3 interacted with both G. max RESPONSE REGULATOR 18a (GmRR18a) and GmMYC2a to inhibit their transcriptional activation of cytokinin oxidase gene G. max CYTOKININ OXIDASE 3-4 (GmCKX3-4), which usually affects seed traits. Meanwhile, the GmRR18a binds to the promoter of GmMYC2a and activates GmMYC2a gene expression. In GmJAZ3-overexpressing soybean seeds, the protein contents were increased while the fatty acid contents were reduced compared to those in the control seeds, indicating that the GmJAZ3 affects seed size/weight and compositions. Natural variation in JAZ3 promoter region was further analyzed and Hap3 promoter correlates with higher promoter activity, higher gene expression and higher seed weight. The Hap3 promoter may be selected and fixed during soybean domestication. JAZ3 orthologs from other plants/crops may also control seed size and weight. Taken together, our study reveals a novel molecular module GmJAZ3-GmRR18a/GmMYC2a-GmCKXs for seed size and weight control, providing promising targets during soybean molecular breeding for better seed traits.

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The GATA transcription factor TaGATA1 recruits demethylase TaELF6‐A1 and enhances seed dormancy in wheat by directly regulating TaABI5

Xuening Wei, Yuyan Li, Xiuliang Zhu, Xin Liu, Xingguo Ye, Miaoping Zhou and Zengyan Zhang

J Integr Plant Biol 2023, 65 (5): 1262-1276.
DOI: 10.1111/jipb.13437

Abstract (Browse 236) |

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Seed dormancy is an important agronomic trait in crops, and plants with low dormancy are prone to preharvest sprouting (PHS) under high‐ temperature and humid conditions. In this study, we report that the GATA transcription factor TaGATA1 is a positive regulator of seed dormancy by regulating TaABI5 expression in wheat. Our results demonstrate that TaGATA1 overexpression significantly enhances seed dormancy and increases resistance to PHS in wheat. Gene expression patterns, abscisic acid (ABA) response assay, and transcriptome analysis all indicate that TaGATA1 functions through the ABA signaling pathway. The transcript abundance of TaABI5, an essential regulator in the ABA signaling pathway, is significantly elevated in plants overexpressing TaGATA1. Chromatin immunoprecipitation assay (ChIP) and transient expression analysis showed that TaGATA1 binds to the GATA motifs at the promoter of TaABI5 and induces its expression. We also demonstrate that TaGATA1 physically interacts with the putative demethylase TaELF6‐ A1, the wheat orthologue of Arabidopsis ELF6. ChIP–qPCR analysis showed that H3K27me3 levels significantly decline at the TaABI5 promoter in the TaGATA1‐overexpression wheat line and that transient expression of TaELF6‐A1 reduces methylation levels at the TaABI5 promoter, increasing TaABI5 expression. These findings reveal a new transcription module, including TaGATA1– TaELF6‐A1–TaABI5, which contributes to seed dormancy through the ABA signaling pathway and epigenetic reprogramming at the target site. TaGATA1 could be a candidate gene for improving PHS resistance.

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Cited: Web of Science(3)

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Sdr4 dominates pre-harvest sprouting and facilitates adaptation to local climatic condition in Asian cultivated rice

Bo Zhao, Hui Zhang, Tianxiao Chen, Ling Ding, Liying Zhang, Xiali Ding, Jun Zhang, Qian Qian and Yong Xiang

J Integr Plant Biol 2022, 64 (6): 1246-1263.
doi: 10.1111/jipb.13266

Abstract (Browse 342) |

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Pre-harvest sprouting (PHS), which reduces grain yield and quality, is controlled by seed dormancy genes. Because few dormancy-related genes have been cloned, the genetic basis of seed dormancy in rice (Oryza sativa L.) remains unclear. Here, we performed a genome-wide association study and linkage mapping to dissect the genetic basis of seed dormancy in rice. Our findings suggest that Seed Dormancy4 (Sdr4), a central modulator of seed dormancy, integrates the abscisic acid and gibberellic acid signaling pathways at the transcriptional level. Haplotype analysis revealed that three Sdr4 alleles in rice cultivars already existed in ancestral Oryza rufipogon accessions. Furthermore, like the semi-dwarf 1 (SD1) and Rc loci, Sdr4 underwent selection during the domestication and improvement of Asian cultivated rice. The distribution frequency of the Sdr4-n allele in different locations in Asia is negatively associated with local annual temperature and precipitation. Finally, we developed functional molecular markers for Sdr4, SD1, and Rc for use in molecular breeding. Our results provide clues about the molecular basis of Sdr4-regulated seed dormancy. Moreover, these findings provide guidance for utilizing the favorable alleles of Sdr4 and Rc to synergistically boost PHS resistance, yield, and quality in modern rice varieties.

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Cited: Web of Science(6)

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The MIEL1-ABI5/MYB30 regulatory module fine tunes abscisic acid signaling during seed germination

Kaili Nie, Hongyun Zhao, Xiaopei Wang, Yanli Niu, Huapeng Zhou and Yuan Zheng

J Integr Plant Biol 2022, 64 (4): 930-941.
DOI: 10.1111/jipb.13234

Abstract (Browse 433) |

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The transcription factor ABSCISIC ACID INSENSITIVE5 (ABI5) plays a crucial role in abscisic acid (ABA) signaling during seed germination. However, how ABI5 is regulated during this process is poorly understood. Here, we report that the ubiquitin E3 ligase MIEL1 and its target transcription factor MYB30 modulate ABA responses in Arabidopsis thaliana during seed germination and seedling establishment via the precise regulation of ABI5. MIEL1 interacts with and ubiquitinates ABI5 to facilitate its degradation during germination. The transcription factor MYB30, whose turnover is mediated by MIEL1 during seed germination, also interacts with ABI5 to interfere with its transcriptional activity. MYB30 functions downstream of MIEL1 in the ABA response, and both are epistatic to ABI5 in ABA-mediated inhibition of seed germination and postgerminative growth. ABA treatment induces the degradation of MIEL1 and represses the interaction between MIEL1 and ABI5/MYB30, thus releasing both ABI5 and MYB30. Our results demonstrate that MIEL1 directly mediates the proteasomal degradation of ABI5 and inhibits its activity via the release of its target protein MYB30, thus ensuring precise ABA signaling during seed germination and seedling establishment.

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Cited: Web of Science(17)

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New insights into cell–cell communications during seed development in flowering plants

Wei Wang, Hanxian Xiong, Kaiting Sun, Bo Zhang and Meng‐Xiang Sun

J Integr Plant Biol 2022, 64 (2): 215-229.
doi: 10.1111/jipb.13170

Abstract (Browse 346) |

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The evolution of seeds is a major reason why flowering plants are a dominant life form on Earth. The developing seed is composed of two fertilization products, the embryo and endosperm, which are surrounded by a maternally derived seed coat. Accumulating evidence indicates that efficient communication among all three seed components is required to ensure coordinated seed development. Cell communication within plant seeds has drawn much attention in recent years. In this study, we review current knowledge of cross-talk among the endosperm, embryo, and seed coat during seed development, and highlight recent advances in this field.

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Cited: Web of Science(14)

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Natural alleles of a uridine 5ʹ-diphospho-glucosyltransferase gene responsible for differential endosperm development between upland rice and paddy rice

Zihao Wu, Xiao Zhang, Guimei Chang, Jun Yang, Jinpeng Wan, Feijun Wang, Dayun Tao, Jiawu Zhou, Lianguang Shang, Peng Xu and Diqiu Yu

J Integr Plant Biol 2022, 64 (1): 135-148.
doi: 10.1111/jipb.13184

Abstract (Browse 271) |

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Traditional upland rice generally exhibits insufficient grains resulting from abnormal endosperm development compared to paddy rice. However, the underlying molecular mechanism of this trait is poorly understood. Here, we cloned the uridine 5ʹ-diphospho (UDP)-glucosyltransferase gene EDR1 (Endosperm Development in Rice) responsible for differential endosperm development between upland rice and paddy rice by performing quantitative trait loci analysis and map-based cloning. EDR1 was highly expressed in developing seeds during grain filling. Natural variations in EDR1 significantly reduced the UDP-glucosyltransferase activity of EDR1^YZN compared to EDR1^YD1, resulting in abnormal endosperm development in the near-isogenic line, accompanied by insufficient grains and changes in grain quality. By analyzing the distribution of the two alleles EDR1^YD1 and EDR1^YZN among diverse paddy rice and upland rice varieties, we discovered that EDR1 was conserved in upland rice, but segregated in paddy rice. Further analyses of grain chalkiness in the alleles of EDR1^YD1 and EDR1^YZN varieties indicated that rice varieties harboring EDR1^YZN and EDR1^YD1 preferentially showed high chalkiness, and low chalkiness, respectively. Taken together, these results suggest that the UDP-glucosyltransferase gene EDR1 is an important determinant controlling differential endosperm development between upland rice and paddy 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 366) |

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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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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 514) |

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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, Wx^mw, 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 Wx^mw may have derived from recombination between two important natural Wx alleles, Wxⁱⁿ and Wx^b. We validated the effects of Wx^mw on rice grain quality using both transgenic lines and near‐isogenic lines (NILs). When introgressed into the japonica Nipponbare (NIP) background, Wx^mw resulted in a moderate AC that was intermediate between that of NILs carrying the Wx^b allele and NILs with the Wx^mp allele. Notably, mature grains of NILs fixed for Wx^mw had an improved transparent endosperm relative to soft rice. Further, we introduced Wx^mw 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 Wx^mw 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 Wx^la 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 497) |

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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, Wx^la, which combined two mutations from Wx^b and Wxⁱⁿ, exhibited a unique phenotype. Reduced GBSSI activity conferred Wx^la rice with both a transparent appearance and good eating quality. Haplotype analysis revealed that Wx^la 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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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 339) |

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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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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 376) |

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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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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 226) |

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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 242) |

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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 377) |

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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

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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 389) |

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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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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 542) |

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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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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 357) |

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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 442) |

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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 280) |

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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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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 266) |

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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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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 351) |

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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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The root microbiome: Community assembly and its contributions to plant fitness

Bo Bai, Weidong Liu, Xingyu Qiu, Jie Zhang, Jingying Zhang and Yang Bai

J Integr Plant Biol 2022, 64 (2): 230-243.
doi: 10.1111/jipb.13226

Abstract (Browse 528) |

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The root microbiome refers to the community of microbes living in association with a plant's roots, and includes mutualists, pathogens, and commensals. Here we focus on recent advances in the study of root commensal community which is the major research object of microbiome-related researches. With the rapid development of new technologies, plant–commensal interactions can be explored with unprecedented breadth and depth. Both the soil environment and the host plant drive commensal community assembly. The bulk soil is the seed bank of potential commensals, and plants use root exudates and immune responses to build healthy microbial communities from the available microbes. The plant microbiome extends the functional system of plants by participating in a variety of processes, including nutrient absorption, growth promotion, and resistance to biotic and abiotic stresses. Plants and their microbiomes have evolved adaptation strategies over time. However, there is still a huge gap in our understanding of the regulatory mechanisms of plant–commensal interactions. In this review, we summarize recent research on the assembly of root microbial communities and the effects of these communities on plant growth and development, and look at the prospects for promoting sustainable agricultural development through the study of the root microbiome.

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Cited: Web of Science(56)

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Rice FLOURY ENDOSPERM22, encoding a pentatricopeptide repeat protein, is involved in both mitochondrial RNA splicing and editing and is crucial for endosperm development

Hang Yang, Yunlong Wang, Yunlu Tian, Xuan Teng, Zehui Lv, Jie Lei, Erchao Duan, Hui Dong, Xue Yang, Yuanyan Zhang, Yinglun Sun, Xiaoli Chen, Xiuhao Bao, Rongbo Chen, Chuanwei Gu, Yipeng Zhang, Xiaokang Jiang, Wenyu Ma, Pengcheng Zhang, Yi Ji, Yu Zhang, Yihua Wang and Jianmin Wan

J Integr Plant Biol 2023, 65 (3): 755-771.
DOI: 10.1111/jipb.13402

Abstract (Browse 267) |

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Most of the reported P-type pentatricopeptide repeat (PPR) proteins play roles in organelle RNA stabilization and splicing. However, P-type PPRs involved in both RNA splicing and editing have rarely been reported, and their underlying mechanism remains largely unknown. Here, we report a rice floury endosperm22 (flo22) mutant with delayed amyloplast development in endosperm cells. Map-based cloning and complementation tests demonstrated that FLO22 encodes a mitochondrion-localized P-type PPR protein. Mutation of FLO22 resulting in defective trans-splicing of mitochondrial nad1 intron 1 and perhaps causing instability of mature transcripts affected assembly and activity of complex Ⅰ, and mitochondrial morphology and function. RNA-seq analysis showed that expression levels of many genes involved in starch and sucrose metabolism were significantly down-regulated in the flo22 mutant compared with the wild type, whereas genes related to oxidative phosphorylation and the tricarboxylic acid cycle were significantly up-regulated. In addition to involvement in splicing as a P-type PPR protein, we found that FLO22 interacted with DYW3, a DYW-type PPR protein, and they may function synergistically in mitochondrial RNA editing. The present work indicated that FLO22 plays an important role in endosperm development and plant growth by participating in nad1 maturation and multi-site editing of mitochondrial messager RNA.

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Cited: Web of Science(2)

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