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Orchestration of Three Transporters and Distinct Vascular Structures in Node for Intervascular Transfer of Silicon in Rice

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Orchestration of Three Transporters and Distinct Vascular Structures in Node for Intervascular Transfer of Silicon in Rice Orchestration of three transporters and distinct vascular structures in node for intervascular transfer of silicon in rice Naoki Yamajia,1, Gen Sakuraib,1, Namiki Mitani-Uenoa, and Jian Feng Maa,2 aInstitute of Plant Science and Resources, Okayama University, Kurashiki 710-0046, Japan; and bEcosystem Informatics Division, National Institute for Agro-Environmental Sciences, Tsukuba 305-8604, Japan Edited by Maarten J. Chrispeels, University of California, San Diego, La Jolla, CA, and approved July 27, 2015 (received for review May 7, 2015) Requirement of mineral elements in different plant tissues is not After EVB phase, the VB is continued to a VB of the leaf asso- often consistent with their transpiration rate; therefore, plants ciating the node (2–4). As an exception, DVBs in the uppermost have developed systems for preferential distribution of mineral two nodes (nodes I and II), in which VBs have no corresponding elements to the developing tissues with low transpiration. Here leaves, become VBs in the panicle without EVB phase as detailed we took silicon (Si) as an example and revealed an efficient system in ref. 2. Based on these repetitive vascular constructions, inter- for preferential distribution of Si in the node of rice (Oryza sativa). vascular transfers between axial VBs are required for preferential Rice is able to accumulate more than 10% Si of the dry weight in delivery of nutrients to apical tissues such as developing leaf or the husk, which is required for protecting the grains from water panicle (2). Furthermore, the node also shows distinct structures at loss and pathogen infection. However, it has been unknown for a cellular and subcellular level, which are characterized by (i)ex- long time how this hyperaccumulation is achieved. We found that panded xylem area of EVBs; (ii) differentiation of xylem transfer three transporters (Lsi2, Lsi3, and Lsi6) located at the node are cells (XTCs), which have expanded cell surface due to cell wall involved in the intervascular transfer, which is required for the ingrowth facing to the xylem vessel; (iii) increased number of preferential distribution of Si. Lsi2 was polarly localized to the DVBs around the EVBs; and (iv) parenchyma cell bridge (PCB) bundle sheath cell layer around the enlarged vascular bundles, with dense plasmodesmata between EVB and DVB (2, 4, 5). PLANT BIOLOGY which is next to the xylem transfer cell layer where Lsi6 is local- However, the role of these structures in intervascular transfer of ized. Lsi3 was located in the parenchyma tissues between en- nutrients has not been examined. larged vascular bundles and diffuse vascular bundles. Similar to In the present study, we examined the preferential distribution Lsi6, knockout of Lsi2 and Lsi3 also resulted in decreased distribu- system of silicon (Si) in rice. Silicon, the most abundant mineral tion of Si to the panicles but increased Si to the flag leaf. Further- element, shows beneficial effects for plant growth (6). The more, we constructed a mathematical model for Si distribution and beneficial effects are characterized by protecting plants from revealed that in addition to cooperation of three transporters, an abiotic and biotic stresses (6). Silicon is especially important for apoplastic barrier localized at the bundle sheath cells and devel- high and sustainable production of rice (Oryza sativa), a typical Si opment of the enlarged vascular bundles in node are also required accumulating species. Rice is able to accumulate Si up to 10% of for the hyperaccumulation of Si in rice husk. the shoot dry weight, which is severalfold more than macronu- trients such as nitrogen, phosphorus, and potassium (7). Low node | rice transporter | apoplastic barrier | silicon distribution | accumulation of Si in rice results in significant reduction of the mathematical model yield (8); therefore, Si fertilization has been considered as a lants have different requirement for mineral elements Significance Pdepending on organs and tissues. For examples, developing tissues such as new leaves and reproductive organs require more Requirement of mineral elements differs with different organs mineral elements for their active growth (1). However, these tissues and tissues; therefore, plants have developed systems for usually have low transpiration; therefore, transpiration-dependent preferentially delivering mineral elements to tissues with high distribution of mineral elements is not sufficient to meet their high requirement. However, the molecular mechanisms for these requirements. Plants must have developed systems for preferential systems are poorly understood. We took silicon (Si) as an ex- distribution of mineral elements depending on the requirements. ample and revealed an efficient distribution system occurring However, the molecular mechanisms for these systems are poorly in the node of rice, which is a hub for distribution. We found understood. Recently, several studies have shown that nodes func- that hyperaccumulation of Si in the husk (more than 10%) is tion as a hub for distribution of mineral elements in graminaceous achieved by cooperation of three different Si transporters lo- plants (2). calized at the different cell layers in the node. Furthermore, Node is a key component of the phytomer in graminaceous mathematical modeling showed that an apoplastic barrier and plants, which is connected with a leaf, a tiller (or a tiller bud), and development of enlarged vascular bundles are also required. crown roots (or these primordia) to the culm or panicle (2, 3). Our work revealed a set of players for efficient distribution Therefore, graminaceous plants are composed of repeated nodes. control in node. Nodes have apparently complicated but regularly organized vas- cular bundles (VBs). No VBs are continuously connected from the Author contributions: N.Y. and J.F.M. designed research; N.Y., G.S., N.M.-U., and J.F.M. per- bottom to the top of the culm, but a unit of VB is repeated with a formed research; N.Y., G.S., N.M.-U., and J.F.M. analyzed data; and N.Y., G.S., and J.F.M. wrote two-thirds overlapped rule; one axial VB is connected with three the paper. nodes and a leaf and specialized at different nodes as diffuse VB The authors declare no conflict of interest. (DVB), transit VB (TVB), and enlarged VB (EVB) from basal to This article is a PNAS Direct Submission. apical (2, 3). In a node, three different axial VBs with different 1N.Y. and G.S. contributed equally to this work. phases coexist and connected transversely by nodal vascular anas- 2To whom correspondence should be addressed. Email: [email protected]. tomosis (NVA). TVB is a passage phase, but its appearance and This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. function within the node are similar to one of the multiple DVBs. 1073/pnas.1508987112/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1508987112 PNAS | September 8, 2015 | vol. 112 | no. 36 | 11401–11406 Downloaded by guest on September 29, 2021 practice of rice production in many countries, especially under A heavy application of nitrogen fertilizers (7). SIET3 SIET4 SIET5 Silicon in soil solution is present in the form of silicic acid, an m Lsi1 Lsi6 Lsi2 Lsi3 500 uncharged molecule (7). Silicic acid is taken by the roots through 400 300 two different transporters: Lsi1 and Lsi2 in rice (9, 10). Lsi1 be- 200 longs to NIP subgroup of aquaporin and preamble to silicic acid, 100 whereas Lsi2 is an efflux transporter of silicic acid (9, 10). Both Lsi1 and Lsi2 are localized at the exodermis and endodermis cells of rice roots, but in contrast to Lsi1, which is localized at the distal B Caryopsis side, Lsi2 is localized at the proximal side (9, 10). Knockout of Rachis either Lsi1 or Lsi2 results in defect of Si uptake (9, 10). Recently, in Peduncle silico mathematical modeling revealed that in addition to co- Node I operation of Lsi1 and Lsi2, presence of the Casparian strips at the Node II exodermis and endodermis is also required for efficient Si uptake Node III and high accumulation (11). Unelongated stem After uptake, more than 95% of Si is rapidly translocated from the roots to the shoots (7). Silicon is also present in the form of 0.0 0.5 1.0 1.5 silicicacidinthexylemsap(12), which is unloaded by Lsi6, a Relative expression homolog of Lsi1 (13). Lsi6 is polarly localized in the adaxial side of the xylem parenchyma cells in the leaf sheaths and leaf blades (13). With water loss due to transpiration, silicic acid is gradually con- C Caryopsis centrated and polymerized to amorphous silica, which is deposited Rachis beneath the cuticle, forming cuticle–silica double layers, and inside Peduncle of particular cells of leaf epidermis (motor cells and short silica Node I cells) (7). Knockout of Lsi6 results in leakage of large amount of Node II silicic acid into the leaf guttation and altered deposition of Si in the Node III leaves (13). Unelongated stem At the reproductive stage, higher Si is finally deposited in the husk, which can reach more than 10% of the dry weight (7). 0.0 0.5 1.0 1.5 Silicon in the husk is also deposited between the epidermal cell Relative expression wall and the cuticle, forming a cuticle–silica double layer (7). This heavy deposition of Si in the husk is very important for rice Fig. 1. Expression analysis. (A) Semiquantitative RT-PCR of Lsi1-like genes grain fertility because it prevents water loss and pathogen (e.g., (Lsi1 and Lsi6) and Lsi2-like genes (Lsi2, Lsi3, SIET3, SIET4, and SIET5) in node – I of rice sampled at the heading stage. PCR products (25 cycle) with ladder panicle blast) infection (6 8). However, the question arises on marker (m) were electrophoresed and stained by ethidium bromide.
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