The functional evolution of geranyl diphosphate synthases with different architectures

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Song, Jin, Chen, He, Li, Tang, et al. establish that independent evolutionary processes in ancestral land plants led to homo- and heteromeric geranyl diphosphate synthases.

Shuyan Song and Shan Lu

School of Life Sciences, Nanjing University, Nanjing 210023, China

Background: Terpenoids are a large group of plant natural products that include small, volatile compounds that contribute to plant aroma (e.g., linalool, limonene, pinene), plant hormones (gibberellins, strigolactones, abscisic acid), carotenoids, and massive compounds that constitute natural rubber. Terpenoids are built with the 5-carbon (C5) precursors isopentenyl diphosphate (IPP) and dimethylallyl diphosphate (DMAPP). Plants use IPP and DMAPP at a 1:1 ratio to synthesize geranyl diphosphate (GPP) and 3:1 ratio to synthesize geranylgeranyl diphosphate (GGPP). GPP is a substrate for making volatile monoterpenes, which plants use to adapt to surrounding environments. GGPP is an intermediate for producing carotenoids, chlorophylls, and other compounds critical for plant survival. GGPP synthases (GGPPSs) exist in all plants, but GPP synthases (GPPSs) are rare in plants other than gymnosperms. Angiosperms generally use Type I small subunit proteins (SSUIs) to have GGPPS produce GPP. There are also Type II SSUs (SSUIIs), which enhance the functions of GGPPS. GPPSs, GGPPSs and SSUs share high sequence similarities. GPPSs and GGPPSs can form homodimers, and GGPPS can also form heterodimers with SSUs.

Question: How did angiosperms develop the strategy of using the GGPPS/SSU combination, instead of genuine GGPPSs and GPPSs, to regulate terpenoid metabolism. How did GPPSs and SSUs evolve?

Findings: By analyzing GGPPS homologs from many photosynthetic organisms, we found GGPPS gene family expansion and functional divergence experienced by ancestral nonvascular plants. This allowed independent parallel evolutionary processes to form genuine GPPSs in gymnosperms and SSUIs in angiosperms. We also found that a pair of amino acids determine the product difference between GPPSs and GGPPSs.

Next steps: At the evolutionary and physiological levels, we want to prove that the GGPPS/SSUI strategy utilized in angiosperms gives plants greater flexibility in modulating terpenoid metabolism, compared with gymnosperms that use separate GGPPS and GPPS, which directly compete for IPP and DMAPP.

Reference:

Shuyan Song, Ruitao Jin, Yufan Chen, Sitong He, Kui Li, Qian Tang, Qi Wang, Linjuan Wang, Mengjuan Kong, Natalia Dudareva, Brian J. Smith, Fei Zhou, Shan Lu. (2023). The functional evolution of architecturally different plant geranyl diphosphate synthases from geranylgeranyl diphosphate synthase. https://doi.org/10.1093/plcell/koad083

SWEET11b transports sugar and cytokinins in barley grains

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Radchuk et al. explore the physiological role of SWEETs in barley grain development.

By Volodymyr Radchuk and Ljudmilla Borisjuk

Leibniz-Institute of Plant Genetics and Crop Plant Research (IPK), Gatersleben, Germany

Background: Sugars Will Eventually be Exported Transporter (SWEET) is a large family of proteins, which have been found in every sequenced plant genome. The main function of SWEET proteins is the transport of sugars like sucrose and glucose. This makes SWEETs important for various processes during a plant’s growth and development. However, the SWEET family in barley was not characterized so far either in terms of its capabilities to transport specific substrates or their functional roles in grain’s growth and development.

Questions: What is the physiological role of SWEETs in barley grain development? Which substrates are transported by the SWEET proteins present in the seed?

Findings: Of 23 barley SWEET genes, HvSWEET11b, HvSWEET15a and HvSWEET4 are predominantly active in the developing grains. HvSWEET11b protein functions not only as a sugar transporter but is able also to transport the phytohormone cytokinin. Plants carrying a knockout homozygous mutation of HvSWEET11b failed to set any viable grain. The partial repression of HvSWEET11b transcription altered the allocation of both sucrose and cytokinin in the grain and resulted in fewer endosperm cells, lower starch and protein accumulation, and a reduction of the grain size at maturity. The dual substrate capacity of a single transporter protein provides the plant with an efficient means of coordinating the grain’s development and filling.

Next steps: This study highlights the relevance of SWEET proteins as multifunctional transporters. It would be of great interest to explore the molecular mechanisms of how cytokinin transport and metabolism towards and in the grains influence their development.

Reference:

Volodymyr Radchuk, Zeinu M. Belew, Andre Gündel, Simon Mayer, Alexander Hilo, Goetz Hensel, Rajiv Sharma, Kerstin Neumann, Stefan Ortleb, Steffen Wagner, Aleksandra Muszynska, Christoph Crocoll, Deyang Xu, Iris Hoffie, Jochen Kumlehn, Joerg Fuchs, Fritz F. Peleke, Jedrzej J. Szymanski, Hardy Rolletschek, Hussam H. Nour-Eldin, Ljudmilla Borisjuk. (2023). SWEET11b transports both sugar and cytokinin in developing barley grains. https://doi.org/10.1093/plcell/koad055

Antagonistic regulation of tomato branching

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Wang et al. revealed fine regulation of inflorescence branching in tomato. The Plant Cell (2023).

By X.T. Wang and X. Cui

Background: The number of branches in the inflorescence affects yield in food crops and the aesthetics of ornamental plants. Two MADS-box transcription factors, SISTER OF TM3 (STM3) and JOINTLESS2 (J2), are tomato homologs of Arabidopsis SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 and SEPALLATA 4, respectively, and have opposing regulatory functions in controlling inflorescence branching.

Question: How do STM3 and J2 antagonistically regulate inflorescence branching in tomato?

Findings: We used chromatin immunoprecipitation followed by high-throughput sequencing (ChIP-seq) and electrophoretic mobility shift assays (EMSA) to identify and confirm a set of common putative target genes that are directly bound by STM3 and J2 via the CArG box motif in their promoter regions. One of these direct targets, FRUITFULL1 (FUL1), is antagonistically regulated by STM3 and J2 during inflorescence development. STM3 forms a complex with J2 and mediates its translocation from the cytosol to the nucleus, thus restricting J2 repressor activity. J2 also limits STM3 function by repressing STM3 expression and inhibits its binding activity. Our results suggest an antagonistic regulatory mode in which STM3 and J2 exert flexible control over inflorescence meristem determinacy and branch number.

Next steps: We and others aim to identify additional factors affecting tomato inflorescence development and the environmental adaptability of inflorescence branching.

Reference:

Xiaotian Wang, Zhiqiang Liu, Jingwei Bai, Shuai Sun, Jia Song, Ren Li, Xia Cui. (2023). Antagonistic regulation of target genes by the SISTER OF TM3–JOINTLESS2 complex in tomato inflorescence branching. https://doi.org/10.1093/plcell/koad065

Wheat Grain Research Goes Translational Regulation

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Guo, Chen, Peng, and colleagues study the translational regulation of gene expression during grain development in bread wheat.

By Yiwen Guo, Yongming Chen, and Huiru Peng

Frontiers Science Center for Molecular Design Breeding, Key Laboratory of Crop Heterosis and Utilization, Beijing Key Laboratory of Crop Genetic Improvement, China Agricultural University, Beijing 100193, China.

 Background: Bread wheat (Triticum aestivum) is one of the most widely cultivated cereal crops worldwide and provides most of the calories consumed by humans. DNA contains the genetic codes and is first transcribed to produce mRNAs, which are then translated to produce proteins. Translational regulation is a widespread mechanism that rapidly modulates gene expression to maintain growth and development. The current investigations into gene regulation in wheat grains focus on the transcriptional level, neglecting the translational level.

Question: How is gene expression regulated at the translational level in developing wheat grains? What functional proteins are involved in grain development?

Findings: We used two approaches, namely ribosome profiling and polysome profiling, to obtain a unique translatome dataset of developing bread wheat grain. The translation of many functional genes is modulated in a stage-specific manner. The divergence of the translational regulation between the wheat subgenomes is pervasive, which increases the expression flexibility of allohexaploid wheat. Widespread, previously unannotated open reading frames (ORFs) are actively expressed in wheat grains. Upstream open reading frames (uORFs) as translational regulatory elements can repress or even activate the translation of mRNAs. Gene translation may be combinatorially modulated by uORFs, downstream ORFs, and microRNAs.

Next steps: Our work presents valuable translatomic resources for understanding the translational control of gene expression during wheat grain development. Further studies will explore functional translational regulatory elements to improve wheat yield and quality.

Reference:

Yiwen Guo, Yongming Chen, Yongfa Wang, Xiaojia Wu, Xiaoyu Zhang, Weiwei Mao, Hongjian Yu, Kai Guo, Jin Xu, Liang Ma, Weilong Guo, Zhaorong Hu, Mingming Xin, Yingyin Yao, Zhongfu Ni, Qixin Sun, and Huiru Peng. (2023). The translational landscape of bread wheat during grain development. https://doi.org/10.1093/plcell/koad075

 

题目：小麦籽粒发育的翻译调控图谱

Guo、Chen和Peng等人在The Plant Cell在线发表了题为“The translational landscape of bread wheat during grain development”的研究论文，构建了小麦籽粒发育的翻译组图谱，揭示了籽粒发育过程的翻译调控机制。

背景回顾：

小麦是世界范围内最重要的谷类作物之一，为人类提供了所需的能量和蛋白质。遗传信息首先转录产生mRNA，然后翻译产生蛋白质。在小麦的生长发育过程中，翻译水平上的基因表达调控发挥着重要作用。然而，当前对小麦籽粒的研究主要集中在转录水平，对翻译调控了解甚少。

科学问题：

在小麦籽粒发育过程中，基因表达在翻译水平是如何被调控的？哪些功能蛋白参与了籽粒发育过程的翻译调控？

研究发现：

该研究利用核糖体谱和多聚核糖体谱分析技术构建了小麦籽粒发育的翻译组图谱。发现许多功能基因的表达在不同籽粒发育阶段被特异地翻译调控。小麦亚基因组间部分同源基因的翻译调控发生分化，从而提高了异源六倍体小麦的表达可塑性。此外，研究发现小麦籽粒中存在许多未知的开放阅读框（ORF）。上游ORF（uORF）可以抑制甚至增强基因的翻译，扮演着翻译调控元件的角色。基因翻译可能受到uORF、下游ORF和microRNA的共同调控。

展望未来：

该研究构建了小麦籽粒翻译调控图谱，加深了对籽粒发育过程中翻译水平上基因表达调控的认识。未来的研究将对翻译调控元件进行更多的功能分析，并将其应用于小麦品种改良。

Focus Issue: Biomolecular Condensates

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Although The Plant Cell Focus Issue on Biomolecular Condensates officially comes out in September, due to the idiosyncrasies of publishing many of the articles are already available online, and I’m highlighting them now because this topic is also the focus of a plenary session at the Plant Biology meeting in August (https://plantbiology.aspb.org/plenaries/). Although the term “biomolecular condensates” is relatively new, it actually reflects a convergence and synthesis of several distinct threads of research. Biomolecular condensates span from “classic” membraneless organelles (e.g., nucleolus, pyrenoid) to small, transient functional condensates, some of which are only recently recognized. I particularly enjoyed reading about how membranes can be involved in the formation of some of these condensates, revealing yet again that cells are stunningly sophisticated systems. A lot of the advancements in our understanding come from new tools and imaging techniques that reveal condensate structures and functions, many of which are reviewed here. The collection provides a great overview of this coalescing discipline, and it’s one not to miss. Start with the editorial overview by Gutierrez-Beltran et al. (Summary by Mary Williams @PlantTeaching) Plant Cell 10.1093/plcell/koad182

Spotlight: Salt and Peppers

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In my cruise around the internet looking for fascinating plant science, I found this tasty morsel. It’s a Spotlight feature of new paper on the effects of salt stress on plants of the genus Capsicum. I don’t want to detract from author Robert Calderon’s fine writing, so head over to Physiologia Plantarum for the story of “Salt and peppers — two spices meet to turn up the heat”. (Summary by Mary Williams @PlantTeaching) Physiologia Plantarum. Spotlight by Calderon 10.1111/ppl.13967 describing new work by Shams et al. 10.1111/ppl.13889.

Soluble and insoluble α-glucan synthesis in yeast by enzyme suites derived from maize endosperm

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Starch is a polymer of α-glucose which is assembled into insoluble, semi-crystalline granules in plants. It is not known why we see only insoluble starch granules in plants and no soluble α-glucan polymers. To investigate this, Boehlein et al. took a synthetic biology approach. Eleven starch metabolism genes from maize endosperm were expressed in differing combinations in a yeast strain with impaired glycogen metabolism (so as not to interfere with starch synthesis). Expression of the starch debranching enzyme ISA1 promoted the formation of insoluble α-glucan polymers and a reduction in the amount of soluble α-glucan polymers. The most striking change occurred in a strain expressing five starch synthase genes and the starch phosphorylase PHO1. Expressing ISA1 in this strain increased the amount of insoluble α-glucan polymers from 16% to 82%. The structure of these insoluble α-glucan polymers was investigated with scanning and transmission electron microscopy. In strains without ISA the particles had an oblate shape whilst strains containing ISA had particles which were more spherical. Therefore, this synthetic biology system has elucidated the role of ISA1 in promoting insoluble starch granule formation and influencing granule morphology. This system could be exploited further by expressing other factors involved in starch granule formation. (Summary by Rose McNelly @Rose_McN) Plant Physiol.  10.1093/plphys/kiad358

Grasses exploit geometry for improved guard cell dynamics

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Stomata are pores on the surface of leaves essential for gas exchange. In grasses, stomatal aperture is controlled by pairs of dumbbell shaped guard cells, with each guard cell surrounded by a subsidiary cell. Despite cell geometry being well described, it was unclear how it influences stomata function. Here, Durney et al. used confocal imaging to visualize stomatal opening and stomatal closure in barley leaves. Using these data they derived a finite element model for barley stomata. They show that when subsidiary cell pressure was set to a constant value, no matter whether high or low, the stomata still functioned. However, removing subsidiary cells from the model prevented complete stomatal closure, showing the importance of subsidiary cells in this process. They experimentally tested this by imaging stomata from the Brachypodium distachyon bdmute mutant, which lacks subsidiary cells, and deriving additional mathematical models. The authors also used the mathematical models to investigate cell wall anisotropy in barley guard cells. When anisotropy was set at an orthogonal angle or removed completely, the stomata had normal pressure-aperture response curves, suggesting that guard cell anisotropy is not important for stomatal function. Therefore, this study dissects the role of cell geometry in grass stomatal function and emphasizes the power of combining computational and wet lab techniques. (Summary by Rose McNelly @Rose_McN) Curr. Biol. 10.1016/j.cub.2023.05.051

Interconnected: Hydrotropism and phototropism in Arabidopsis root growth

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Tropisms enable plants to shift their growth direction in response to environmental changes. The roots of Arabidopsis plants respond to gravity by growing in the direction of gravity, a phenomenon known as gravitropism, while in response to unilateral blue light they bend away, demonstrating phototropism. Additionally, roots respond to moisture gradients by moving toward areas with greater water availability, resulting in hydrotropism. In this research article, Lei Pang and colleagues investigate the function of the proteins MIZ1 (MIZU-KUSSEI) and GNOM/MIZ2, which were previously isolated as ahydrotropic mutants, and attempt to determine their role in phototropic and hydrotropic responses of Arabidopsis roots. The study shows that MIZ1 has a role in recovering a complete phototropic response and hydrotropic response in Arabidopsis roots when expressed in the cortex of the elongation zone in miz1. The expression of GNOM in tissues- epidermis, cortex, or stele, is required for the full induction of these tropic responses in the roots. The function of MIZ1 and GNOM in the tissue elongation zone suggests a crosstalk between these tropisms. The discovery of MIZ1 and GNOM/MIZ2 as key actors in both hydrotropism and phototropism sheds light on how various environmental stimuli are coordinated during root growth. This study adds to our understanding of how plants use information from their surroundings to improve their growth and development. (Summary by Arpita Yadav arpita_yadav_). J. Exp. Bot. 10.1093/jxb/erad193