How do root hairs keep their tubular shape?

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Hirano et al. uncover the secretion route for root hair shank hardening in Arabidopsis. The Plant Cell (2023).

https://doi.org/10.1093/plcell/koad240

By T. Hirano, K. Ebine, T. Ueda, T. Higaki, T. W.-Nakayama, H. Konno, H. T.-Imamura, and M. H. Sato

Background: Root hairs are rapidly growing tubular projections of root epidermal cells and play an essential role in plant water and nutrient uptake. Root hair formation involves tip growth and the concomitant hardening of the shank by producing a secondary cell wall layer to form an elongated tubular structure.

Question: The polarized secretion of materials in the root hair tip has been well studied. However, little is known about the secretion of secondary cell wall materials in the root hair shank.

Findings: We observed increased localization of SYP123 at the plasma membrane of the subapical and shank zones compared to the tip region in elongating root hairs. Inhibition of PtdIns(3,5)P2 production impaired SYP123 localization in the plasma membrane and SYP123-mediated root hair shank hardening, and root hair elongation in syp123 mutant is insensitive to the PtdIns(3,5)P2 synthesis inhibitor. SYP123 interacts with both VAMP721 and VAMP727. The syp123 and vamp727 mutants exhibited reduced shank cell wall stiffness due to impaired secondary cell wall components deposition. In conclusion, the SYP123/VAMP727-dependent secretion system delivers secondary cell wall components for hardening the subapical zone and shank of Arabidopsis root hairs.

Next steps: Further studies are needed to confirm the detailed molecular mechanisms underlying the multiple secretion pathways for root hair morphogenesis.

Reference:

Tomoko Hirano, Kazuo Ebine, Takashi Ueda, Takumi Higaki, Takahiro Watanabe-Nakayama, Hiroki Konno, Hisako Takigawa-Imamura, and Masa H. Sato. The SYP123-VAMP727 SNARE complex is involved in the delivery of secondary cell wall components for hardening the root hair shank in Arabidopsis https://doi.org/10.1093/plcell/koad240

Microtubule-associated proteins regulate tomato fruit shape

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Bao et al. reveal how microtubule-associated proteins regulate tomato fruit shape formation from a cell biology perspective.

 Plant Cell https://doi.org/10.1093/plcell/koad231

 Zhiru Bao and Pengwei Wang

National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, Hubei Province, China; 2. Hubei Hongshan Laboratory, Wuhan 430070, China

Background: Genes encoding microtubule-binding proteins have emerged as conserved trait loci for fruit shape regulation with important roles during domestication. While microtubule-binding proteins have been reported in many fruit crops, most studies were performed using forward genetics or population genetics approaches. Thus, in-depth molecular and cell biology insight is lacking.

Question: How are cortical microtubules organized in fruit tissue? From a cell biology perspective, which proteins regulate microtubule dynamics and organization in tomato fruits?

Findings: We identified the microtubule-associated proteins SlMAP70s and SlIQD21a as important regulators of tomato fruit shape. These proteins interact and affect microtubule stability, which may contribute to the re-arrangement of cortical microtubules and cell growth patterns underlying organ shape. Transgenic tomato lines over-expressing SlMAP70-1 produced elongated fruits with reduced cell circularity and microtubule anisotropy, while loss-of-function mutants exhibited flatter fruits. Fruits were further elongated in plants co-expressing both SlMAP70-1 and SlIQD21a.

Next steps: These findings shed light on the functional regulation of microtubule organization and provide a powerful approach for future studies on fruit shape regulation in fruit crops.

Reference:

Zhiru Bao, Ye Guo, Yaling Deng, Jingze Zang, Junhong Zhang, Yingtian Deng, Bo Ouyang, Xiaolu Qu, Katharina Bürstenbinder and Pengwei Wang. (2023) Microtubule-associated protein SlMAP70 interacts with IQ67-domain protein SlIQD21a to regulate fruit shape in tomato. https://doi.org/10.1093/plcell/koad231

Stepwise cell fate establishment in the rice stem

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Tsuda et al. investigate the temporal order of cell fate establishment during stem development in rice.

https://doi.org/10.1093/plcell/koad241

By Katsutoshi Tsuda

Background: The stem, which consists of nodes and internodes, is an axis of the shoot that physically supports lateral organs such as leaves and flowers and enables water transport and solute exchange. In contrast to other organs such as leaves, roots, and flowers, stem development remains poorly understood. In seed plants, the stem is produced from the shoot apical meristem as a part of the developmental unit called the phytomer, which comprises a leaf, a stem, and an axillary bud.

Question: In what temporal order is cell fate established for each organ in a phytomer? To address this question, we developed a heat shock-inducible clonal analysis system in rice (Oryza sativa). By introducing clonal sectors at various time points during flag leaf phytomer development, we examined whether the fate of a given cell is determined for a certain organ.

An immature stem of the flag leaf phytomer, consisting of node I, internode II, and foot II.

Findings: We found that cell fate establishment occurs stepwise for each organ. First, phytomer founder cells are determined before leaf initiation from the shoot apical meristem. Next, the fate of the node is determined in the meristem flank, splitting cell lineages destined for the leaf and the stem. Axillary bud cell fate is established shortly after leaf initiation. Finally, the cell population destined for internodes emerges from, at most, a few cell tiers in the stem. Therefore, the internode develops last in the phytomer.

Next steps: The molecular mechanisms governing early stem development are largely unknown. We demonstrated that there are distinct steps in phytomer development, and thus, the molecular features (e.g., gene expression) that characterize each step can now be determined experimentally. Developmental mutants with altered plant height can also provide insights into stem development.

 

Reference:

Katsutoshi Tsuda, Akiteru Maeno and Ken-Ichi Nonomura. (2023). Heat-shock inducible clonal analysis reveals the stepwise establishment of cell fates in the rice stem. https://doi.org/10.1093/plcell/koad241

Key factors that interactively regulate maize endosperm development

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Wu et al. explore how three key transcription factors co-regulate gene networks and the regulatory landscape associated with endosperm development and seed phenotype in maize.

 https://doi.org/10.1093/plcell/koad247

Hao Wu1,2 and Philip W. Becraft1,3

  1. Iowa State University, Genetics, Development & Cell Biology Department, Ames, IA;
  2. Cornell University (Current), School of Integrative Plant Science, Ithaca, NY;
  3. Iowa State University, Agronomy Department, Ames, IA

Background: The endosperm of cereal plants such as rice (Oryza sativa) and maize (Zea mays) serves as a storage tissue for nutrients, supplying energy for germination and the initial growth of seedlings. It is also a source for human food, livestock feed, and industrial applications. The endosperm develops in two stages, a cellular development phase characterized by extensive cell division and cell differentiation, and a second phase, grain filling, in which these cells accumulate storage materials, particularly starches and proteins. Three key transcription factors, NAKED ENDOSPERM1 (NKD1), NKD2, and OPAQUE2 (O2), play important roles in maize endosperm cellular development and storage material accumulation. The mutants of these factors showed several common defects in endosperm grain-filling, and this suggests that they may have some related functions. However, we know little about how the three factors interactively regulate downstream genes and the regulatory landscapes that modulate endosperm development.

Question: How do NKD1, NKD2 and O2 co-regulate gene networks and the regulatory landscape associated with endosperm development and how do they interact to control seed phenotype?

Findings: We developed a set of homozygous lines consisting of nkd1, nkd2 and o2 mutants in all single, double, and triple mutant combinations, as well as wild type. We identified synthetic phenotypes suggesting that the three factors interactively affect endosperm development. We found that the three factors may constrain hormone responses, cell wall organization, as well as other cellular developmental processes, and promote starch metabolism, lipid storage, and storage protein accumulation during the transition from cellular development to storage compound accumulation. These processes are regulated through a dynamic, hierarchical gene network and the three factors function as the central regulators. We also reported potential direct target genes of NKD1 and NKD2 along with their chromatin accessibility status and differentially expressed genes between wild type and each mutant.

Next steps: In the future, we plan to test some key direct targets of NKD1 and NKD2 by developing mutant lines to further explore how they work together to regulate endosperm development.

Reference:

Hao Wu, Mary Galli, Carla J. Spears, Junpeng Zhan, Peng Liu, Ramin Yadegari, Joanne M. Dannenhoffer, Andrea Gallavotti, Philip W. Becraft (2023). NAKED ENDOSPERM1, NAKED ENDOSPERM2, and OPAQUE2 interact to regulate gene networks in maize endosperm development. https://doi.org/10.1093/plcell/koad247

Variegated grape berries enlighten us about plant radiation responses

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Zhang et al. identify a regulatory hub in grapevine controlling divergent specialized metabolic pathways as part of the light/UV radiation response.

Plant Cell.  https://doi.org/10.1093/plcell/koad228

By José Tomás Matus and Chen Zhang

Institute for Integrative Systems Biology (I2SysBio), Universitat de València-CSIC, 46980 Paterna, Valencia, Spain.

Background: Since plants made the move to land, they have had to adapt to exposure to high-intensity light and ultraviolet radiation. Anthocyanins that accumulate in epidermal cells shield plant tissues from radiation; the absence of these red/purple pigments negatively affects photosynthesis and other physiological processes. We identified and compared pigmented and unpigmented sections of rare, variegated grapevine (Vitis vinifera) berries to see whether different light responses were occurring in red and white skin sections.

Question: What are the causes and effects of berry color variegation? Does a central genetic switch contribute to the abundance of phenylpropanoids and isoprenoids in variegated berries? Can we integrate computational analyses and experimental evidence to disentangle these questions?

Findings: White variegation in red-skinned grapevine fruits is caused by the presence of non-functional alleles of MYBA1/A2 transcription factors that naturally control anthocyanin biosynthesis. The absence of these pigments enhances a ripening-dependent regulatory network mediated by MYB24 that promotes protection against ultraviolet and high-light intensity stress. In response, white skin sections accumulate higher levels of antioxidant monoterpenes and UV-shielding flavonols; however, these compounds only partially ameliorate the detrimental effects of excessive radiation. Genes related to carotenoid metabolism, photosynthesis and other light signaling responses are bound and directly regulated by MYB24. By conducting in silico and in vitro analyses and using field-grown grapevine plants, we demonstrate that MYB24 orchestrates different specialized metabolism pathways in berry skins in response to increased levels of radiation caused by pigment depletion.

Next steps: Future research should be oriented towards identifying the regulators of MYB24 in order to determine the full regulatory network of MYB24-controlling light responses and late fruit-ripening processes.

Reference:

Chen Zhang, Zhanwu Dai, Thilia Ferrier, Luis Orduña, Antonio Santiago, Arnau Peris, Darren C. J. Wong, Christian Kappel, Stefania Savoi, Rodrigo Loyola, Alessandra Amato, Bartosz Kozak, Miaomiao Li, Akun Liang, David Carrasco, Carlos Meyer-Regueiro, Carmen Espinoza, Ghislaine Hilbert, Rosa Figueroa-Balderas, Dario Cantu, Rosa Arroyo-Garcia, Patricio Arce-Johnson, Patricia Claudel, Daniel Errandonea, Manuel Rodríguez-Concepción, Eric Duchêne, Shao-shan Carol Huang, Simone Diego Castellarin, Giovanni Battista Tornielli, Francois Barrieu, José Tomás Matus (2023). MYB24 orchestrates terpene and flavonol metabolism as light responses to anthocyanin depletion in variegated grape berries. https://doi.org/10.1093/plcell/koad228

Arabidopsis long non-coding RNAs: an orchestrated hubbub

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Kornienko  et al. discover that Arabidopsis genome is full of long-non-coding RNAs that show their expression only in specific tissues and plants from different geographic origins because of differences in epigenetic silencing of these genes.

Plant Cell – https://doi.org/10.1093/plcell/koad233

By Aleksandra E. Kornienko

Background: Only a small fraction of the genome encodes proteins. We were interested in a special type of gene called long non-coding RNAs (lncRNAs): They are transcribed from the genome but do not encode proteins. LncRNAs can regulate genes or organize cell structures but are largely not studied, and we know very little about lncRNAs as a gene class. For example, we know lncRNAs evolve very quickly and are different between species, but we do not know well how they differ within one species and what is responsible for this difference.

Question: We wanted to know how many lncRNAs are present in the model plant Arabidopsis (Arabidopsis thaliana), how they differ in plants from different regions, and whether the recently reported widespread epigenetic variation in Arabidopsis underlies this difference. We used many transcriptome and epigenetic sequencing datasets to answer these questions.

Findings: We discovered that the Arabidopsis genome is full of lncRNAs, although most are epigenetically inactivated. Plants from different regions have different sets of active lncRNAs, and epigenetic differences are responsible for much of this difference. Intergenic lncRNAs were particularly variable in their expression levels and contained pieces of transposons, selfish genes that can move and propagate in the genome. Cells fight the spread of transposons with elaborate systems inactivating them and preventing them from harming the genome. We determined that these transposon pieces made lncRNAs look like transposons and become inactivated by the same system.

Next steps: It is unclear what underlies the epigenetic variation causing lncRNA variation; is it a difference in sequence, or the absence of the whole lncRNA gene from the genomes of Arabidopsis from certain regions? What contributes the most? Another direction is to understand the nature and origin of transposon pieces inside lncRNAs.

Reference: 

Aleksandra E. Kornienko, Viktoria Nizhynska, Almudena Molla Morales, Rahul Pisupati, Magnus Nordborg (2023) Population-level annotation of lncRNAs in Arabidopsis reveals extensive expression variation associated with transposable element-like silencing. https://doi.org/10.1093/plcell/koad233

 

Phenotypic and genomic changes during modern wheat breeding in China and the United States

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Jianqing Niu et al. explore how modern breeding reshaped wheat phenotype and genome in China and the United States, which will facilitate breeding higher performance wheat in the future.

https://doi.org/10.1093/plcell/koad229

By Jianqing Niu and Hong-Qing Ling from Hainan Yazhou Bay Seed Laboratory and Institute of Genetics and Developmental Biology, Chinese Academy of Sciences.

Background: A landrace is a traditional plant variety capable of tolerating local biotic and abiotic stresses and maintaining intermediate yield levels in low-input farming systems. The development of cultivars from landraces was achieved by human-mediated selection aimed at higher yield, better quality, and stronger fitness. The transition from landraces to elite cultivars is regarded as crop improvement, during which beneficial alleles might gradually accumulate in cultivars. Therefore, understanding the genetic architecture of wheat improvement during the transition from landraces to cultivars in distinct geographic regions will be crucial for developing high-performance varieties in the future.

Question: How has modern wheat breeding reshaped the phenotypic and genomic architecture of wheat in China and the United States?

Findings: We performed a comprehensive comparative analysis (at the phenotypic and genomic levels) of a whole-genome resequencing panel of 355 common wheat accessions representing diverse landraces and modern cultivars from China and the United States. Compared with landraces, the genetic diversity, and phenotypes of modern wheat cultivars from China and the United States changed significantly. Furthermore, we identified breeding targets during modern wheat breeding and determined that breeding for increased productivity in these two geographic regions was accomplished by pyramiding both shared and region-specific variants.

Next steps: The unique loci selected either in China or the United States can be used to develop high-performance wheat varieties in the future.

Reference:

Jianqing Niu, Shengwei Ma, Shusong Zheng, Chi Zhang, et al. (2023). Whole-genome sequencing of diverse wheat accessions uncovers genetic changes during modern breeding in China and the United States. https://doi.org/10.1093/plcell/koad229

 

题目：现代育种对小麦表型和基因组的重塑

背景：约8000多年前，小麦起源于新月沃地，然后逐渐向世界各地传播。在传播过程中形成地方品种，它们能够适应当地环境和胁迫，且在相对较低的投入下保持中等产量。近代小麦育种是对地方品种进行改良，使其成为高产、优质和适应性更强的品种。此过程可能对小麦的表型以及基因组进行极大的重塑。在不同的小麦生产区，可能由于当地气候以及育种者的喜好差异，会培育出截然不同的品种。因此，比较分析现代育种对不同地域的小麦表型和基因组的重塑，可以为培育更加优良的小麦新品种提供重要线索。

问题：现代育种如何重塑中美两国小麦的表型和基因组？

发现：通过对355份来自中国和美国的品种以及其它地区的地方品种进行表型评价和重测序分析发现，与地方品种相比，现代品种表型和遗传多态性均发生了很大的改变，且优异等位基因逐渐积累。此外，还对中美两国的育种靶标进行了分析，鉴定出了中美共有以及独有的育种靶标。

展望未来：他山之石，可以攻玉。将本文鉴定到的优良育种靶标导入到栽培品种，可进一步改良现有品种，增强环境胁迫的适应性，提高产量和品质。

A MATE transporter regulates grain size in rice

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Zhou et al. discover a molecular mechanism of rice grain size regulation.

https://doi.org/10.1093/plcell/koad239

By Chunlei Zhou from Nanjing Agricultural University

Background: Grain size is a key factor for determining grain yield. Many genes or quantitative trait loci (QTLs) that regulate grain size have been identified. Among them, members of the CYP78A cytochrome P450 subfamily are conserved regulators of grain (seed) size in plants. However, the relation between CYP78As and other grain size regulators is largely unknown. Although CYP78As have been reported to likely function by generating a mobile growth signal, the underlying molecular mechanism remains elusive.

Question: What is the regulatory pathway of grain size involving CYP78As? What is the molecular and genetic mechanism behind it?

Figure: A proposed working model for SMG4’s role in regulating rice grain size. A) CYP78As may catalyze and generate a growth signal (CYP78A-derived signal) in the ER, and SMG4 interacts with CYP78As to receive the CYP78A-derived signal. Then, SMG4 interacts with COPII components to transmit the CYP78A-derived signal from the ER to Golgi. B) In WT, CYP78A-derived signals are transported from the ER to Golgi normally to promote cell expansion and cell proliferation in spikelet hulls, thus leading to normal grains. In smg4, the transport of CYP78A-derived signal from the ER to Golgi is disrupted, thus restricting cell expansion and cell proliferation in spikelet hulls and finally leading to small grains.

 

Findings: Here we identified a MATE transporter, SMALL GRAIN 4 (SMG4), that regulates grain size in rice. Loss of function of SMG4 causes smaller grains, while overexpressing SMG4 results in larger grains. SMG4 is mainly localized to ER exit sites (ERESs) and partially localized to the endoplasmic reticulum and Golgi. Biochemical assays showed that SMG4 interacts with CYP78As (BG2, GRAIN LENGTH 3.2 [GL3.2], and BG2-LIKE 1 [BG2L1]) and COPⅡ components (Sar1, Sec23, and Sec24). Genetic analyses suggest that CYP78As, SMG4, and Sar1 likely act, at least in part, in a common pathway to regulate grain size. Taken together, our findings reveal that a CYP78As–SMG4–COPⅡ pathway promotes grain size in rice, thus providing a new strategy for improving grain size and yield in crops.

Next step：We will further investigate the nature of the CYP78A-derived signal transported by SMG4, and reveal how it is transmitted.

Reference:

Chunlei Zhou, Qibing Lin, Yulong Ren, Jie Lan, Rong Miao, Miao Feng, Xin Wang, Xi Liu, Shengzhong Zhang, Tian Pan, Jiachang Wang, Sheng Luo, Jinsheng Qian, Wenfan Luo, Changling Mou, Thanhliem Nguyen, Zhijun Cheng, Xin Zhang, Cailin Lei, Shanshan Zhu, Xiuping Guo, Jie Wang, Zhichao Zhao, Shijia Liu, Ling Jiang, and Jianmin Wan (2023). A CYP78As–small grain4–coat protein complex Ⅱ pathway promotes grain size in rice. https://doi.org/10.1093/plcell/koad239

Review. Milestones in understanding phosphorus uptake, transport, sensing, use, and signaling

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Phosphorus (P) is an essential nutrient and critical component of nucleic acids, phospholipids, and other molecules. Yang et al. provide a historical (since 1996) overview of the processes controlling its uptake and use. Plants take up P from the rhizosphere primarily in the form of orthophosphate (Pi). However, Pi in the soil often complexes with metal ions, limiting its availability. The discovery in 1996 of root-specific PHT1 phosphate transporters, localized in the plasma membrane and induced during Pi deficiency, initiated extensive exploration into this vital nutrient element. Subsequent identification of Pi transporters with expression in various tissues (e.g. stele, reproductive tissue, embryo) or subcellular organelles (e.g. chloroplasts/plastids, mitochondria, Golgi apparatus, vacuole) highlighted their role in mediating Pi uptake, cell-to-cell movement, and long-distance transport, thereby ensuring a balance between internal homeostasis and external supply and ultimately maximizing plant performance. Achieving this homeostasis demands a complex interplay of diverse and sophisticated molecular regulatory mechanisms including microRNAs, transcription factors, untranslated open reading frames, the ubiquitin ligase system, protein phosphorylation, and ligand-regulated protein-protein interactions. Furthermore, recent breakthroughs elucidating the structural-functional relationship of the regulatory PP-InsP/SPX/PHR complex not only enhance our understanding of the P signaling cascade but also unveil exciting opportunities for the interplay between P signaling and other crucial physiological processes, including nitrogen and iron homeostasis, and the dynamics of plant-microbe interactions. (Summary by Ching Chan @ntnuchanlab) Plant Cell 10.1093/plcell/koad326