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Home , Phloem

COMMENTARY

The secret of pumpkins

Robert Turgeona and Karl Oparkab,1 aDepartment of , Cornell University, Ithaca, NY 14853; and bInstitute of Molecular Plant Sciences, University of Edinburgh, Edinburgh EH9 3JR, United Kingdom

he phloem of higher laterally in the stem and petiole (Fig. 1). transports the products of pho- Now, using video microscopy and phloem- T tosynthesis and other nutrients labeling techniques, Zhang et al. (4) show over long distances from that the fascicular phloem quickly becomes to sink tissues, such as , tubers, and blocked when the stem is cut. In contrast, , where they are used in growth or the extrafascicular phloem bleeds profusely storage. The primary conducting cells of for many minutes, indicating that it does the phloem are the enucleate sieve ele- not have the “normal” sealing systems ments, which are intimately connected to found in other types of phloem. Their data their neighboring companion cells. The point to the fact that most studies of the sieve elements are joined at their ends by metabolite, protein, and RNA composition perforated walls called sieve plates to of the cucurbit phloem probably relate to form sieve tubes, through which solutes the contents of the relatively minor extra- flow as a river of nutrient solution. Many fascicular sieve elements and not the main recent studies have focused on the fasci- conducting phloem elements of the stem. nating discovery that the phloem functions Their results also explain a long-standing not only to transport low-molecular– conundrum, namely, why the con- weight solutes but also , tent of cucurbit is about 30-fold less including proteins and . The con- than the requirements of photosynthate ducting phloem has been likened to the delivery.Whentheylookedindetailat plant’s “superhighway” (1), delivering the fascicular phloem using dis- a broad range of defense and develop- section and microsampling techniques, mental signals to distant parts of the plant, they found that the fascicular sieve ele- including the flowering signal “florigen” ments do indeed contain up to 1 M sug- and the signal for tuberization in potatoes ars, which is sufficientforfruitgrowth, (2, 3). These concepts form the foundation whereas the extrafascicular phloem con- of a unique and exciting field in develop- tains only low (millimolar) levels of sug- mental biology. ars. Significantly, they also show that the fi Fig. 1. Transverse section of a C. maxima stem As a tissue, the phloem is dif cult to (redrawn from ref. 7). The fascicular phloem (pink) protein composition of the divergent study because it is under extremely high occurs on either side of the (gray) in the phloem systems differs markedly. pressure as a result of the elevated con- main vascular bundles of the stem. The extra- Why does the extrafascicular phloem centrations of solutes it carries. Severing fascicular phloem (blue) forms an anastomosing not seal immediately to prevent release of the phloem results in massive disruption of network in the (pale green) and also in the sieve element contents? In most plants, sieve element contents and surging of the (dark green). A detailed description of cu- wound sealing of the sieve plate pores is curbit anatomy is provided by Crafts (6). displaced materials onto the sieve plate. achieved by deposition of callose (a wound As a result, the sieve plate pores plug, carbohydrate present around the sieve making it difficult to sample the phloem plate pores) as well as by the surge of cell these species has made them a popular and analyze the molecules it conducts. contents, mostly filamentous phloem pro- choice in studies of phloem transport and This has challenged researchers to look for teins (P-proteins), into the pores (7). Clues in determining the composition of the unique sampling methods that do not dis- as to why extrafascicular sieve elements conducting sieve elements. A common as- turb the delicate sieve elements. One do not block came from ultrastructural way of doing this is to use phloem-feeding sumption made in these studies is that studies in the 1960s (reviewed in ref. 8) insects, such as , that “tap” the phloem sap represents the contents of the showing that the sieve plates of the extra- contents of the conducting phloem. By vascular (conducting) phloem and, there- fi fascicular sieve elements are characterized severing the stylet with a laser (laser fore, that the molecules identi ed in sap by a relative lack of callose. Kempers “stylectomy”), it is possible to collect and are representative of those in long- et al. (8) subsequently made use of this analyze nanoliter samples of sap derived distance transit. property to deliver macromolecules into directly from the conducting sieve tubes. In PNAS, Zhang et al. (4) show that the cut extrafascicular phloem of Cu- However, not all aphid/plant combinations the exuding phloem sap of cucurbits is curbita maxima. They found that simply “ ” yield sap, and the collection method is derived from the so-called extrafascicular by dipping the cut end of the stem into both difficult and time-consuming. A sec- phloem and not the vascular (fascicular) fluorescent dextrans, macromolecules ond approach is to use plant species in conducting phloem of the vascular bun- were taken up and transported along the which the phloem “bleeds,” that is, re- dles. The fact that the cucurbits have two extrafascicular sieve elements. In the leases sieve element contents after the types of phloem was recognized, anatom- phloem has been severed. The Cucurbita- ically, over two centuries ago (5, 6). The ceae (cucurbits) contains several members, fascicular phloem is restricted to either Author contributions: R.T. and K.O. wrote the paper. including pumpkin, melon, and cucumber, side of the xylem in the main vascular The authors declare no conflict of interest. that exude copious amounts of phloem bundles, whereas the extrafascicular See companion article on page 13532. sap after cutting the stem. The ease with phloem forms an anastomosing network 1To whom correspondence should be addressed. E-mail: which phloem sap can be collected from that interconnects the vascular bundles [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1008134107 PNAS | July 27, 2010 | vol. 107 | no. 30 | 13201–13202 Downloaded by guest on September 26, 2021 study by Zhang et al. (4), P-proteins were range of unidentified secondary metabo- phloem systems will prove to manifest it- found in the extrafascicular phloem; how- lites. Because the extrafascicular phloem is self more subtly in the phloem of other ever, surprisingly, the fascicular phloem common near the and through- higher plants. However, the recent release had very low levels of P-proteins, and yet out the stem, it may provide strategic rings of the complete cucumber genome se- this phloem blocks almost instantaneously of defense against pathogens. In this case, quence (9) will provide a platform for on wounding. They speculate that some of having a phloem system that bleeds pro- further interesting studies on the unusual the other major proteins identified in the fusely to release defense compounds may phloem of the Cucurbitaceae. Although fascicular phloem may perform the wound- inhibit pathogens and protect the sugar- transcriptome, proteome, and metab- sealing functions of the fascicular phloem. rich fascicular phloem from insect and olome data on cucurbit exudate are un- What then is the function of the enig- fungal attack. doubtedly important in the study of the matic extrafascicular phloem? It does not A final question is whether the cucurbits extrafascicular phloem and its functions, appear to be involved in loading are unique in evolving two functionally for analysis of sap involved in long-distant into the phloem of source leaves because it different transport systems. As pointed out transit from source to sink tissues, it may is absent from the minor veins of leaves, by Zhang et al. (4), this runs contrary to be wise to use other systems in which ex- the main sites of phloem loading. Zhang the widely held belief that the phloem of udate appears to come directly from the fi et al. (4) speculate that it may be involved higher plants represents a uni ed conduit moving translocation stream (10). in plant defense against pathogens. They for the translocation of metabolites. It re- found the extrafascicular phloem sap to mains to be shown whether the extreme ACKNOWLEDGMENTS. We are grateful to Jessica contain abundant amino acids and a wide division of labor shown by the cucurbit Fitzgibbon for drawing Fig. 1.

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13202 | www.pnas.org/cgi/doi/10.1073/pnas.1008134107 Turgeon and Oparka Downloaded by guest on September 26, 2021