William J. Lucas

• Chair at University of California, Davis

In flowering plants, inferior ovaries are key morphological innovations that evolved multiple times from superior ovaries to protect female parts of the flower. However, the developmental mechanisms underlying inferior ovary formation remain largely unknown. Comparative spatial transcriptome mapping and cell lineage reconstructions in developing fl...

The tetraploid genome and clonal propagation of the cultivated potato (Solanum tuberosum L.)1,2 dictate a slow, non-accumulative breeding mode of the most important tuber crop. Transitioning potato breeding to a seed-propagated hybrid system based on diploid inbred lines has the potential to greatly accelerate its improvement³. Crucially, the devel...

Root-synthesized secondary metabolites are critical quality-conferring compounds of foods, plant-derived medicines, and beverages. However, information at a single-cell level on root-specific secondary metabolism remains largely unexplored. L -Theanine, an important quality component of tea, is primarily synthesized in roots, from which it is then...

Root-synthesized secondary metabolites are critical quality-conferring compounds of foods, plant-derived medicines, and beverages. However, information at a single-cell level on root-specific secondary metabolism remains largely unexplored. L-theanine, an important quality component of tea, is primarily synthesized in roots, from which it is then t...

Legumes acquire nitrogen-fixing ability by forming root nodules. Transferring this capability to more crops could reduce our reliance on nitrogen fertilizers, thereby decreasing environmental pollution and agricultural production costs. Nodule organogenesis is complex, and a comprehensive transcriptomic atlas is crucial for understanding the underl...

Root-synthesized secondary metabolites are critical quality-conferring compounds of foods, plant-derived medicines, and beverages. However, information at a single-cell level on root-specific secondary metabolism remains largely unexplored. L-theanine, an important quality component of tea, is primarily synthesized in roots, from which it is then t...

Root-synthesized secondary metabolites are critical quality-conferring compounds of foods, plant-derived medicines, and beverages. However, information at a single-cell level on root-specific secondary metabolism remains largely unexplored. L-theanine, an important quality component of tea, is primarily synthesized in roots, from which it is then t...

Under depleted external phosphate (Pi), many plant species adapt to this stress by initiating downstream signalling cascades. In plants, the vascular system delivers nutrients and signalling agents to control physiological and developmental processes. Currently, limited information is available regarding the direct role of phloem-borne long-distanc...

Root system architecture (RSA) plays a pivotal role in efficient uptake of essential nutrients, such as phosphorous (P), nitrogen (N), and water. In soils with heterogeneous nutrient distribution, root plasticity can optimize acquisition and plant growth. Here, we present evidence that a constitutive RSA can confer benefits for sorghum grown under...

Plasmodesmata (PD) are plasma membrane (PM)-lined cytoplasmic nanochannels that mediate in cell-to-cell communication across the cell wall. A range of proteins are embedded in the PD PM and endoplasmic reticulum (ER) and function in regulating PD-mediated symplasmic trafficking. However, knowledge of the nature and function of the ER-embedded prote...

Membrane‐localized transporters constitute important components for specialized metabolism in plants. However, due to the vast array of specialized metabolites produced by plants, and the large families of transporter genes, knowledge about the intracellular and intercellular transport of plant metabolites is still in its infancy. Cucurbitacins are...

Euphyllophytes encompass almost all extant plants, including two sister clades, ferns and seed plants. Decoding genomes of ferns is the key to deep insight into the origin of euphyllophytes and the evolution of seed plants. Here we report a chromosome-level genome assembly of Adiantum capillus-veneris L., a model homosporous fern. This fern genome...

Underground microbial ecosystems have profound impacts on plant health1–5. Recently, essential roles have been shown for plant specialized metabolites in shaping the rhizosphere microbiome6–9. However, the potential mechanisms underlying the root-to-soil delivery of these metabolites remain to be elucidated10. Cucurbitacins, the characteristic bitt...

Organic tea is more popular than conventional tea that originates from fertilized plants. Amino acids inorganic soils constitute a substantial pool nitrogen (N) available for plants. However, the amino-acid contents in soils of tea plantations and how tea plants take up these amino acids remain largely unknown. In this study, we show that the amino...

Theanine, one of the most important components of teas, confers the umami taste and relaxation effect of tea infusion. As a non‐proteinogenic amino acid, theanine solely accumulates to high levels in tea plants (Camellia sinensis L.); however, the underlying mechanism remains largely unknown. Theanine is biosynthesized from ethylamine and glutamate...

Potato is the third most important staple food crop. To address challenges associated with global food security, a hybrid potato breeding system, aimed at converting potato from a tuber-propagated tetraploid crop into a seed-propagated diploid crop through crossing inbred lines, is under development. However, given that most diploid potatoes are se...

Shading was thought as an effective approach to increase theanine in harvested tea shoots. Previous studies offered conflicting findings, perhaps since the integration of theanine metabolism and transport in different tissues was not considered. Theanine is synthesized primarily in the roots and is then transported, via the vascular system, to new...

Unisexual flowers provide a useful system for studying plant sex determination. In cucumber (Cucumis sativus L.), three major Mendelian loci control unisexual flower development, Female (F), androecious [a; 1-aminocyclopropane-1-carboxylate {ACC} synthase 11, acs11], and Monoecious (M; ACS2), referred to here as the Female, Androecious, Monoecious...

Axillary meristem development determines both plant architecture and crop yield; this critical process is regulated by the PROLIFERATING CELL FACTORS (TCP) family of transcription factors. Although TCP proteins bind primarily to promoter regions, some also target gene bodies for expression activation. However, the underlying regulatory mechanism re...

Domesticated crops with high yield and quality are frequently susceptible to pathogen attack, whereas enhancement of disease resistance generally compromises crop yield. The underlying mechanisms of how plant development and disease resistance are coordinately programed remain elusive. Here, we showed that the basic Helix-Loop-Helix (bHLH) transcri...

Axillary meristem development determines both plant architecture and crop yield; this critical process is regulated by the TCP transcription factor (TF) family, including the maize TB1 and Arabidopsis BRC1. Studies have shown that both TB1 and AtBRC1 can target the gene body regions of some target genes and activate their expression; however, the r...

In plants, RNA interference (RNAi) plays a pivotal role in growth and development, and responses to environmental inputs, including pathogen attack. The intercellular and systemic trafficking of small interfering/micro(si/mi)RNA is a central component in this regulatory pathway. Currently, little is known with regards to the molecular agents involv...

The botanical family Cucurbitaceae includes a variety of fruit crops with global or local economic importance. How their genomes evolve and the genetic basis of diversity remain largely unexplored. In this study, we sequence the genome of the wax gourd (Benincasa hispida), which bears giant fruit up to 80 cm in length and weighing over 20 kg. Compa...

The phloem, located within the vascular system, is critical for delivery of nutrients and signaling molecules throughout the plant body. Although the morphological process and several factors regulating phloem differentiation have been reported, the molecular mechanism underlying its initiation remains largely unknown. Here, we report that the smal...

Theanine, a unique non‐proteinogenic amino acid, is an important component of tea, as it confers the umami taste and relaxation effect of tea as a beverage. Theanine is primarily synthesized in tea roots and is subsequently transported to young shoots, which are harvested for tea production. Currently, the mechanism for theanine transport in the te...

In plants, male sterility is an important agronomic trait, especially in hybrid crop production. Many factors are known to affect crop male sterility, but it remains unclear whether Suc transporters (SUTs) participate directly in this process. Here, we identified and functionally characterized the cucumber (Cucumis sativus) CsSUT1, a typical plasma...

In response to phosphate (Pi) deficiency, it has been shown that micro‐RNAs (miRNAs) and mRNAs are transported through the phloem for delivery to sink tissues. Growing evidence also indicates that long non‐coding RNAs (lncRNAs) are critical regulators of Pi homeostasis in plants. However, whether lncRNAs are present in and move through the phloem,...

The sections in this article are Introduction Phloem is Well Suited for Long‐Distance Trafficking of Macromolecules Macromolecular Trafficking in the Phloem Nucleic Acids in the Phloem and Their Role in Long‐Distance Signaling Developmental Regulation Influences the Number and Properties of PD : Impacts on Long‐Distance Trafficking in the Phlo...

The Cucurbita genus contains several economically important species in the Cucurbitaceae family. Here we report high-quality genome sequences of C. maxima and C. moschata and provide evidence supporting an allotetraploidization event in Cucurbita. We are able to partition the genome into two homoeologous subgenomes based on different genetic distan...

The Cucurbita genus contains several economically important species in the Cucurbitaceae family. Interspecific hybrids between C. maxima and C. moschata are widely used as rootstocks for other cucurbit crops. We report high-quality genome sequences of C. maxima and C. moschata and provide evidence supporting an allotetraploidization event in Cucurb...

The plant vascular system plays a central role in coordinating physiological and developmental events through delivery of both essential nutrients and long-distance signaling agents. The enucleate phloem sieve tube system of the angiosperms contains a broad spectrum of RNA species. Grafting and transcriptomics studies have indicated that several th...

In this Special Issue, a focus is also placed on the role of the xylem as an essential conduit for the long-distance delivery of water and mineral nutrients from the soil to the vegetative (above-ground) regions of the plant. Xylem cells destined to form tracheids or vessel members, which will make up the conduit for this water and mineral transpor...

In recent years, considerable attention has been paid to exploring the complex gene regulatory networks involved in the development of the plant vascular system. Such information is crucial to our understanding of the molecular and cellular events which give rise to the integrated tissues of the xylem and phloem, leading to the formation of structu...

The plant vascular system, and specifically the phloem plays a pivotal role in allocation of fixed carbon to developing sink organs. Although the processes involved in loading and unloading of sugars and amino acids are well characterized, in contrast, little information is available regarding the nature of other metabolites in the sieve tube syste...

Depletion of finite global rock phosphate (Pi) reserves will impose major limitations on future agricultural productivity and food security. Hence, modern breeding programmes seek to develop Pi-efficient crops with sustainable yields under reduced Pi fertilizer inputs. In this regard, although the long-term responses of plants to Pi stress are well...

Transcriptional gene silencing is a pivotal mechanism for regulating gene expression and genome stability. In Arabidopsis, combined analyses of small RNAs (sRNAs) and DNA methylation reveals that mobile 24-nt sRNAs are involved in reinforcing genome-wide silencing of transposons through DNA methylation.

Rice is a model plant widely used for basic and applied research programs. Plant cell wall proteins play key roles in a broad range of biological processes. However, presently, knowledge on the rice cell wall proteome is rudimentary in nature. In the present study, the tightly-bound cell wall proteome of rice callus cultured cells using sequential...

It is with profound sadness that we mourn the loss of Dr. Biao Ding, a full-professor in the Department of Molecular Genetics, Ohio State University (OSU), and a world-renowned plant biologist with leading authority in viroid research. He died suddenly on June 26, 2015 in Prague, Czech Republic, while attending the International Conference on Viroi...

The plant vascular system serves as a conduit for the delivery of both nutrients and signaling molecules to the various distantly-located organs. The enucleate sieve tube system of the angiosperm phloem delivers sugars and amino acids to developing organs and, recently, has been shown to contain a unique population of RNA and proteins. Grafting stu...

Transport of photoassimilates from leaf tissues (source regions) to the sink organs is essential for plant development. Here, we show that a phytohormone, the brassinosteroids (BRs) promotes pollen and seed development in rice by directly promoting expression of Carbon Starved Anther (CSA) which encodes a MYB domain protein. Over-expression of the...

Cucurbitacins are triterpenoids that confer a bitter taste in cucurbits such as cucumber, melon, watermelon, squash, and pumpkin. These compounds discourage most pests on the plant and have also been shown to have antitumor properties. With genomics and biochemistry, we identified nine cucumber genes in the pathway for biosynthesis of cucurbitacin...

In plants, the vascular system, and specifically the phloem, functions in delivery of small (s)RNA to exert epigenetic control over developmental and defense-related processes. Although the importance of systemic sRNA delivery has been established, currently, information is lacking concerning the nature of the protein machinery involved in this pro...

RNA silencing is an evolutionarily conserved mechanism triggered by double-stranded RNA that is processed into 21- to 24-nt small interfering (si)RNA or micro (mi)RNA by RNaseIII-like enzymes called Dicers. Gene regulations by RNA silencing have fundamental implications in a large number of biological processes that include antiviral defense, maint...

Plant laccase (LAC) enzymes belong to the blue copper oxidase family and polymerize monolignols into lignin. Recent studies have established the involvement of microRNAs in this process; however, physiological functions and regulation of plant laccases remain poorly understood. Here, we show that a laccase gene, LAC4, regulated by a microRNA, miR39...

As terrestrial plants are sessile organisms and therefore must directly deal with an often complex and changing environment, they have had todevelop complex and elegant strategies to survive and thrive in the face of environmental stress. This is particularly true for plant adaptation to the soil environment, where essential mineral nutrients often...

In plants, auxin functions as a master controller of development, pattern formation, morphogenesis, and tropic responses. A sophisticated transport system has evolved to allow the establishment of precise spatiotemporal auxin gradients that regulate specific developmental programs. A critical unresolved question relates to how these gradients can b...

As an essential plant macronutrient, the low availability of phosphorus (P) in most soils imposes serious limitation on crop production. Plants have evolved complex responsive and adaptive mechanisms for acquisition, remobilization and recycling of phosphate (Pi) to maintain P homeostasis. Spatio-temporal molecular, physiological and biochemical Pi...

The plant vascular system serves a vital function by distributing water, nutrients and hormones essential for growth and development to the various organs of the plant. In this review, attention is focused on the role played by the phloem as the conduit for delivery of both photosynthate and information macromolecules, especially from the context o...

Most fruits in our daily diet are the products of domestication and breeding. Here we report a map of genome variation for a major fruit that encompasses ∼3.6 million variants, generated by deep resequencing of 115 cucumber lines sampled from 3,342 accessions worldwide. Comparative analysis suggests that fruit crops underwent narrower bottlenecks d...

Sadly, Prof. Ko Shimamoto died on September 28, 2013, aged 63. He was born in Wakayama, Japan, on October 19, 1949, received his bachelor's degree in Agriculture from Kyoto University in 1974 and his PhD in Genetics from the University of Wisconsin-Madison in 1980. After his postdoctoral training at the Friedrich Miescher Institut in Basel, Switzer...

Cucurbita moschata FLOWERING LOCUS T-LIKE 2 (hereafter FTL2) and Arabidopsis thaliana (Arabidopsis) FT, components of the plant florigenic signaling system, move long-distance through the phloem from source leaves to the vegetative apex where they mediate floral induction. The mechanisms involved in long-distance trafficking of FT/FTL2 remains to b...

[ William J. Lucas (Corresponding author)] The emergence of the tracheophyte-based vascular system of land plants had major impacts on the evolution of terrestrial biology, in general, through its role in facilitating the development of plants with increased stature, photosynthetic output, and ability to colonize a greatly expanded range of environ...

Cell‐to‐cell trafficking of transcription factors ( TF s) has been shown to play an important role in the regulation of plant developmental events, but the evolutionary relationship between cell‐autonomous and noncell‐autonomous ( NCA ) TF s remains elusive. A t D of4.1 , named INTERCELLULAR TRAFFICKING DOF 1 ( ITD 1 ), was chosen as a representati...

Watermelon, Citrullus lanatus, is an important cucurbit crop grown throughout the world. Here we report a high-quality draft genome sequence of the east Asia watermelon cultivar 97103 (2n = 2× = 22) containing 23,440 predicted protein-coding genes. Comparative genomics analysis provided an evolutionary scenario for the origin of the 11 watermelon c...

In plants, a population of non-cell-autonomous proteins (NCAPs), including numerous transcription factors, move cell to cell through plasmodesmata (PD). In many cases, the intercellular trafficking of these NCAPs is regulated by their interaction with specific PD components. To gain further insight into the functions of this NCAP pathway, coimmunop...

The identification of proteins present in sieve-tube exudate has been urged by the need to unravel the basic cellular processes acting specifically in the sieve elements (SEs) in long-range signaling in defense response and maintenance of enzymatic activities in those enucleate cells. Proteome studies of the sieve-tube exudates have shed new light...

In plants, the phloem is the component of the vascular system that delivers nutrients and transmits signals from mature leaves to developing sink tissues. Recent studies have identified proteins, mRNA, and small RNA within the phloem sap of several plant species. It is now of considerable interest to elucidate the biological functions of these pote...

Endocytosis is essential for the maintenance of protein and lipid compositions in the plasma membrane and for the acquisition of materials from the extracellular space. Clathrin-dependent and -independent endocytic processes are well established in yeast and animals; however, endocytic pathways involved in cargo internalization and intracellular tr...

In plants, cell-to-cell communication is pivotal for the orchestration of cell fate determination, organ development, and the integration of whole plant physiology. One of the strategies for intercellular communication uses symplasmic communication channels, called plasmodesmata (PD). These PD establish unique cytoplasmic channels for the intercell...

Geminiviruses are plant-infecting viruses with small circular single-stranded DNA genomes. These viruses utilize nuclear shuttle proteins (NSPs) and movement proteins (MPs) for trafficking of infectious DNA through the nuclear pore complex and plasmodesmata, respectively. Here, a biochemical approach was used to identify host factors interacting wi...

RNA-binding proteins (RBPs) form ribonucleoprotein (RNP) complexes that play crucial roles in RNA processing for gene regulation. The angiosperm sieve tube system contains a unique population of transcripts, some of which function as long-distance signaling agents involved in regulating organ development. These phloem-mobile mRNAs are translocated...

Phloem-transported signals play an important role in regulating plant development and in orchestrating responses to environmental stimuli. Among such signals, phloem-mobile RNAs have been shown to play an important role as long-distance signaling agents. At maturity, angiosperm sieve elements are enucleate, and thus transcripts in the phloem transl...

Internodal cells of Chara corallina exhibit a spatially controlled pattern of alternating acid and alkaline regions along their surface, corresponding to regions of outward and inward current density, respectively. Incubation of isolated cells in either 25 μg∙mL−1 cycloheximide or 50 μM 2-(4-methyl-2,6-dinitroanilino)-N-methylpropionamide resulted...

The vascular anatomy and phloem ultrastructure of the sugar beet petiole were studied in an attempt to evaluate the potential of petiolar phloem anastomoses to accommodate lateral movement of translocates across this structure. Clearings revealed that six of the eight interveinal regions between the nine major, axially oriented veins were connected...

In plants, plasmodesmata (PD) are intercellular channels that function in both metabolite exchange and the transport of proteins and RNAs. Currently, many of the PD structural and regulatory components remain to be elucidated. Receptor-like kinases (RLKs) belonging to a notably expanded protein family in plants compared to the animal kingdom have b...

In yeast, eIF5A, in combination with eEF2, functions at the translation step, during the protein elongation cycle. This result is of significance with respect to functioning of the enucleate sieve tube system, as eIF5A was recently detected in Cucurbita maxima (pumpkin) phloem sap. In the present study, we further characterized four CmeIF5A isoform...

Cucumber is an economically important crop as well as a model system for sex determination studies and plant vascular biology. Here we report the draft genome sequence of Cucumis sativus var. sativus L., assembled using a novel combination of traditional Sanger and next-generation Illumina GA sequencing technologies to obtain 72.2-fold genome cover...

Land plants have developed highly sophisticated intercellular channels called plasmodesmata (PD) that mediate the cell-to-cell trafficking of signaling molecules, including non-cell autonomous proteins (NCAPs) and RNAs. Until recently, the biological significance of this position-dependent intercellular signaling system was underestimated, as only...

Calmodulin (CaM) is a highly conserved intracellular calcium sensor. In plants, CaM also appears to be present in the apoplasm, and application of exogenous CaM has been shown to influence a number of physiological functions as a polypeptide signal; however, the existence and localization of its corresponding apoplasmic binding sites remain controv...

RNA binding proteins (RBPs) are integral components of ribonucleoprotein (RNP) complexes and play a central role in RNA processing. In plants, some RBPs function in a non-cell-autonomous manner. The angiosperm phloem translocation stream contains a unique population of RBPs, but little is known regarding the nature of the proteins and mRNA species...

Increasing evidence suggests that proteins present in the angiosperm sieve tube system play an important role in the long distance signaling system of plants. To identify the nature of these putatively non-cell-autonomous proteins, we adopted a large scale proteomics approach to analyze pumpkin phloem exudates. Phloem proteins were fractionated by...

The phloem translocation stream of the angiosperms contains a special population of proteins and RNA molecules which appear to be produced in the companion cells prior to being transported into the sieve tube system through the interconnecting plasmodesmata. During this process, these non-cell-autonomous proteins are thought to undergo partial unfo...

The translationally controlled tumor protein (TCTP) is conserved in all eukaryotes studied thus far. Recent evidence points to an important role for TCTP in the induction of cell proliferation in animals through an interaction with G proteins. TCTP may also constitute an intercellular secreted signal that modulates the immune response in the verteb...

IntroductionPhloem is well suited for long-distance trafficking of macromoleculesMacromolecular trafficking in the phloemNucleic acids in the phloem and their role in long-distance signalingDevelopmental regulation influences the number and properties of PD: impacts on long-distance trafficking in the phloemSignaling and systemic defense responsesP...

In plants, cell-to-cell trafficking of non-cell-autonomous proteins (NCAPs) involves protein-protein interactions, and a role for posttranslational modification has been implicated. In this study, proteins contained in pumpkin (Cucurbita maxima cv Big Max) phloem sap were used as a source of NCAPs to further explore the molecular basis for selectiv...

Cucurbita moschata, a cucurbit species responsive to inductive short-day (SD) photoperiods, and Zucchini yellow mosaic virus (ZYMV) were used to test whether long-distance movement of FLOWERING LOCUS T (FT) mRNA or FT is required for floral induction. Ectopic expression of FT by ZYMV was highly effective in mediating floral induction of long-day (L...