(B) Bright-field images of Evans blue-stained wild-type, LexA::D, LexA::ANAC074, LexA::OsD, LexA::NAC1, and LexA::VND6 cells with or without estrogen. Repair of wounds. Taken together, these results indicate that D and its Arabidopsis ortholog, ANAC074, are master transcriptional switches that induce programmed death of stem pith parenchyma cells. NOTE: We only request your email address so that the person you are recommending the page to knows that you wanted them to see it, and that it is not junk mail. 6C). Yonemaru, H.K., T.M., N.T., and S.K. Even Arabidopsis NAC1, which is phylogenetically closest to the D subfamily, does not induce ectopic PCD in Arabidopsis culture cells (Fig. Compartmentalisation: a conceptual framework for understanding how trees grow and defend themselves. Therefore, nonfunctional alleles of D may have been the targets of artificial selection because they improve stem water content and stem strength in sorghum domestication and breeding. Red and blue arrowheads mark representative examples of air bubbles and cellular contents, respectively. Pith parenchyma cells function as a water storage tissue in plant stems, and the death of these cells reduces stem water content. Conflict of interest statement: J.-i. These results strongly suggest that expression of D, ANAC074, or OsD is sufficient to induce cell death in Arabidopsis cells, but NAC1 expression is not sufficient. (F) Hoechst 33342-stained vertical sections of the third internodes in SKS and MS3B stems at 9 WAP. D and ANAC074 encode previously uncharacterized NAC transcription factors and are sufficient to ectopically induce programmed death of Arabidopsis culture cells via the activation of autolytic enzymes. Thus, the discovery of the involvement of the D gene in the programmed death of stem pith parenchyma cells will broadly contribute to agriculture and industry. 6B). 2C). We demonstrated that ANAC074, an Arabidopsis ortholog of D, was preferentially expressed in flowers, older hypocotyls, and older inflorescence stems and that ANAC074 is necessary and sufficient to induce cell death, at least in pith parenchyma of older inflorescence stems. In the trunks of woody plants, the xylem parenchyma cells are colourless and are believed to be involved chiefly in storing starch, oils, and other ergastic substances. Storage of food 4. (F) Cross-sections of the second stem internodes of 74LH3213 at 7–11 WAP. Transcript profiling of the LexA::D and LexA::ANAC074 cell lines (Dataset S2, A and B) showed that induction of D or ANAC074 selectively up-regulated the expression of genes annotated with cysteine-type endopeptidase activity in Gene Ontology terms (SI Appendix, Fig. Pith parenchyma cells store water in various plant organs. White pith parenchyma in the second internode of 74LH3213 stems emerged at 8 WAP, proliferated during 9 and 10 WAP, and became saturated at 11 WAP (Fig. Thus, our study revealed the molecular and cellular mechanism determining stem water content in sorghum and possibly other grasses, crops, and vegetables. 3H, arrowheads). Blue and green dashed lines indicate deletion regions in juicy-stem varieties. Parenchyma is a term used to describe the functional tissues in plants and animals. Error bars show SD (n = 5). Also function in providing support. S3B). 4D), confirming the involvement of D in cell death of stem pith parenchyma. S4). To identify the D gene in sorghum, we used positional cloning and the F2 population from a cross between a dry-stem variety [Senkinshiro (SKS)] and a juicy-stem variety [Nakei MS-3B (MS3B)]. (A) Rough mapping of the D locus. This suggests that ANAC074 induces PCD but not necrosis, in which cells retain cellular organelles even after death (30). Dying pith parenchyma cells were expected to be abundant in the third internode of 74LH3213 stems at 8 WAP (Fig. By contrast, at 48 h after estrogen addition, many of the cells expressing LexA::D, LexA::ANAC074, and LexA::OsD lacked nuclei and plastids (Fig. 5A), and there was no significant difference between the percentage of cells lacking plastids and nuclei in the presence and absence of estrogen (SI Appendix, Fig. 1 F and G), confirming that the latter were dead. 2. These results also highlight differences between D and VND6. Parenchyma cells can function as storage sites for starches, proteins, oils, and so on, and they contribute support to the plant if they are turgid. 2B), referred to as the NAM/ATAF/CUC (NAC) domain (20, 21). 1H, arrowheads). Our data show that D and its Arabidopsis ortholog, ANAC074, are master switches that induce PCD in the stem pith parenchyma. S1), as described previously (15, 17). Parenchyma cells are unique in their meristematic nature. From the Cambridge English Corpus The … (G) Percentage of pith parenchyma cells with Hoechst 33342-stained nuclei (calculated from six 0.25-mm2 images containing ∼24–40 cells) in the third internodes of SKS and MS3B stems at 9 WAP. Parenchyma cells can serve many functions. This means that the cells are pluripotent, having the ability to divide into a number of different cells. In this tissue, only the parenchymatic cell type is present, which shows a thin primary cell wall. Next, we investigated the transactivation activities of D and ANAC074. However, two lines of evidence suggest that the PCD-inducing activity of D subfamily proteins evolved independently of VNS subfamily proteins. Sequence analysis of the Sobic.006G147400 promoter and gene regions in 13 cultivars (four dry-stem cultivars and nine juicy-stem cultivars) indicated that there were at least four alleles (Fig. 2B). 7). Some NAC transcription factors, such as the Arabidopsis VNS subfamily protein VND6 (SI Appendix, Fig. As a result of functional specialization of protoplasts, parenchyma cells may perform assimilative, excretive, and other functions. designed research; M.F., T.S., Y.O., H.K., J.W., H.T., T.O., J.-i. The plasmodesmata and the middle lamella are also commonly present. Author contributions: M.F., J.-i. Arrowheads indicate nuclei. Parenchyma cells and relatively large intercellular spaces in a cross-section through the stem of Geum urbanum. At 30 d after heading (DAH), the amount of juice squeezed from the stems was ∼8 times higher in MS3B than in SKS (Fig. The palisade parenchyma is interpreted as a barrier to desiccation of the acorn and may have a photosynthetic function during the formation of the fruit. 4D), indicating that death was suppressed in pith parenchyma cells but not in tracheary elements. This work was supported by grants from the Ministry of Agriculture, Forestry, and Fisheries of Japan (Genomics for Agricultural Innovation, Grants QTL5503 and QTL5506); the JST [Core Research for Evolutional Science and Technology (CREST), Grant JPMJCR12B5 and PRESTO, Grant JPMJPR11B3]; the Ministry of Education, Culture, Sports, Science and Technology of Japan KAKENHI (Grant 16H01247); and the Japan Society for the Promotion of Science KAKENHI (Grants 16H06172 and 17H05019). (Scale bars: 10 cm and 5 mm in Upper and Lower, respectively, of B; 5 mm in D and F; and 300 μm in H.). Intercellular spaces are present between cells. 3. Image credit: Joyce Gross (University of California, Berkeley). The unifying characteristic of all parenchyma cells is that they are living at maturity and capable of cell division, giving them important roles in regeneration and wound healing. Edited by Richard A. Dixon, University of North Texas, Denton, TX, and approved August 7, 2018 (received for review May 5, 2018). 3B). This strongly suggests that Sobic.006G147400 is the D gene that determines stem water content in sorghum. 4C), providing further evidence that ANAC074 is expressed in these cells. In many flowering plants, the majority of stem pith parenchyma cells die, which leads to the formation of air-filled cavities in the stem (2). There is evidence that pressure exerted by parenchyma in the stem contributes to its growth. These results indicate that D, ANAC074, and OsD specifically induce cell death but do not induce secondary cell-wall formation, unlike VND6. Relative LUC activity in protoplasts transfected with the effector construct harboring CaMV35Spro::::CaMV35Ster (the only regulatory elements) and the reporter construct harboring CEP1pro(−555)::LUC::CaMV35Ster was defined as 1.0. To confirm that D and ANAC074 directly target PCD-related genes, we performed two experiments using the 5′-upstream region of CEP1, a gene that encodes a cysteine peptidase and is up-regulated by expression of D or ANAC074 in Arabidopsis culture cells (Fig. To further explore the relationship between D and stem water content, we compared the expression patterns of D in reproductive stems of a dry-stem variety (74LH3213) and its nearly isogenic line d-NIL. 1D, Upper). Thin walls allow for close packing and rapid diffusion between cells. (C) Subcellular localization of ANAC074-GFP in pith parenchyma cells of 65-d-old inflorescence stem. Expression of ANAC074 under the control of the ANAC074 promoter (SI Appendix, Fig. An initial rough mapping of 54 F2 juicy-stem individuals localized D within a 4.33-Mb region (from 49.7 to 54.0 Mb) on chromosome 6 (Fig. Genome editing technologies can be used to modulate the activity of endogenous D in breeding programs for a range of crops and vegetables. Enter multiple addresses on separate lines or separate them with commas. 3C), where the greatest formation of white pith parenchyma was observed (Fig. Se-Jin Lee and Emily Germain-Lee explain a way to preserve bone and muscle mass during spaceflight. Annual Review of Phytopathology 22: 189–214. Furthermore, unlike VNS subfamily proteins, D subfamily proteins do not appear to be involved in the differentiation of xylem vessels because their loss of function does not affect the PCD of stem tracheary elements, at least in sorghum and Arabidopsis. White arrowheads and red asterisks indicate tracheary elements and pith parenchyma, respectively. 3C). Blue arrows indicate nonfunctional mutation positions. Inhibiting a signaling pathway protects microgravity-exposed mice from losing muscle and bone mass, a study finds. S8, dark purple squares). D expression was spatiotemporally coupled with the appearance of dead, air-filled pith parenchyma cells in sorghum stems. 4A). Most of the SKS pith parenchyma cells are filled with air bubbles, whereas the MS3B pith parenchyma cells retain their cellular contents (Fig. Thus, parenchyma cells play a vital role in the overall development of the plant, throughout its life. For a century, a single gene, long referred to as D, has been proposed to be responsible for determining the juicy- and dry-stem traits of sorghum (13, 14). Vascular plant stems contain three main types of tissues: the outermost dermal tissue protects the internal tissues, vascular tissue transports nutrients and water, and ground tissue stores nutrients and water. We do not capture any email address. 1C). Be on the lookout for your Britannica newsletter to get trusted stories delivered right to your inbox. Second, VNS subfamily proteins are conserved from mosses to flowering plants and are involved in the differentiation of water-conductive and supporting tissues such as hydroid cells, xylem vessels, and xylem fibers (31). The latter consists primarily of parenchyma cells with thin primary cell walls. That means that almost all functions performed in the body of an animal are perfor… Yoneda, K.-i.H., F.I., T.M., S.K., and J.-i. 5A) indicates that genomic DNA is degraded, and strongly supports the proposal that ANAC074 expression induces PCD. Other key functions of these cells include photosynthesis, storage, secretion and transport. In monocots, parenchyma cells fill the large space between dermal and vascular tissues, whereas in dicots they fill the large space inside the ring of vascular tissue (1). Both D and ANAC074 significantly up-regulated expression of the reporter gene (Fig. Consistent with these results, the air porosity of stem tissue (the relative amount of space occupied by air in a given volume of stem tissue) in the third internode of SKS at 9 WAP was ∼8 times higher than that of MS3B (Fig. One experiment was a transactivation assay that used Arabidopsis culture cell protoplasts and a firefly luciferase reporter gene under the control of the CEP1 5′-upstream region. Photosynthesis. Darker cells (Lower) indicate dead air-filled pith parenchyma cells. In animals, the bulk of functional cells in any organ is called the “parenchyma.” This distinguishes the cells which perform the organ’s primary function from “structural” … (D) Evans blue-stained 75-d-old inflorescence stem cross-section images of wild-type, anac074, and anac074 expressing ANAC074-GFP, D-GFP, or OsD-GFP under control of the ANAC074 promoter and terminator regions (anac074 ANAC074pro::ANAC074-GFP, anac074 ANAC074pro::D-GFP, and anac074 ANAC074pro::OsD-GFP). 6D). Like animals, plants have cells that are specialized for different functions. 7). The exchange of gases. 2B). Error bars show SD (n = 3, *P < 0.05, **P < 0.005, ***P < 0.001). wrote the paper. Sorghum (Sorghum bicolor) is a monocot grass that can be used for food, feed, fiber, and fuel production. OsD has 70% identity (76% similarity) with D and 41% identity (50% similarity) with ANAC074. (Lower) Bar graphs represent the relative activities of firefly LUC in Arabidopsis culture cell protoplasts transfected with the indicated combinations of the effector and reporter constructs. The differences between the functions of VNS and D subfamily proteins are consistent with the differences between cellular properties of xylem vessels and dead pith parenchyma cells. function of phloem parenchyma. S6A). Plant tissues PARENCHYMA P arenchyma is not a highly specialized tissue involved in many functions such as photosynthesis, storage, synthesis and processing of many substances, and tissue repairing. S4), can induce PCD (26). Parenchyma may be compact or have extensive spaces between the cells. S4), D subfamily proteins form a clade close to NAC1 subfamily proteins, which is separate from the clade corresponding to VNS subfamily proteins. Plant parenchyma cells make up the bulk of leaves, flowers, and the growing, dividing inner parts of stems and roots. 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