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(12) Patent Application Publication (10) Pub. No.: US 2016/0115499 A1 CUI Et Al US 2016O115499A1 (19) United States (12) Patent Application Publication (10) Pub. No.: US 2016/0115499 A1 CUI et al. (43) Pub. Date: Apr. 28, 2016 (54) MATERALS AND METHODS FOR Publication Classification CONTROLLING BUNDLE SHEATH CELL FATE AND FUNCTION IN PLANTS (51) Int. Cl. CI2N 5/82 (2006.01) (71) Applicant: FLORIDA STATE UNIVERSITY (52) U.S. Cl. RESEARCH FOUNDATION, INC., CPC ........ CI2N 15/8269 (2013.01); C12N 15/8225 Tallahassee, FL (US) (2013.01) (57) ABSTRACT (72) Inventors: HONGCHANG CUI, TALLAHASSEE, The Subject invention concerns materials and methods for FL (US); DANYUKONG, increasing and/or improving photosynthetic efficiency in BLACKSBURG, VA (US); YUELING plants, and in particular, C3 plants. In particular, the Subject HAO, TALLAHASSEE, FL (US) invention provides for means to increase the number of bundle sheath (BS) cells in plants, to improve the efficiency of (21) Appl. No.: 14/898,046 photosynthesis in BS cells, and to increase channels between BS and mesophyll (M) cells. In one embodiment, a method of (22) PCT Fled: Jun. 11, 2014 the invention concerns altering the expression level or pattern of one or more of SHR, SCR, and/or SCL23 in a plant. The (86) PCT NO.: PCT/US2014/041975 Subject invention also pertains to genetically modified plants, S371 (c)(1), and in particular, C3 plants, that exhibit increased expression (2) Date: Dec. 11, 2015 of one or more of SHR, SCR, and/or SCL23. Transformed and transgenic plants are contemplated within the scope of the invention. The Subject invention also concerns methods for increasing expression of photosynthetically important Related U.S. Application Data genes in a plant, wherein one or more genes of interest are (60) Provisional application No. 61/833,771, filed on Jun. operably linked with a plant SHR, SCR or SCL23 promoter 11, 2013. sequence and expressed in a plant. Patent Application Publication Apr. 28, 2016 Sheet 1 of 10 US 2016/0115499 A1 FIG. 1A FIG. 1C F.G. 1E FIG. 1 A-1 FIG. 1C-1 FIG. 1 E-1 Patent Application Publication Apr. 28, 2016 Sheet 2 of 10 US 2016/O115499 A1 FIG. 1B FIG. D FIG. 1 F FIG. 1 B-1 FIG. 1D-1 F.G. 1 F-1 Patent Application Publication Apr. 28, 2016 Sheet 3 of 10 US 2016/O115499 A1 FIG. 2A FG. 2B FIG. 2C FG. 2D FG. 2E FG. 2F FIG. 2G FIG 2H Patent Application Publication Apr. 28, 2016 Sheet 4 of 10 US 2016/0115499 A1 O9**)I,H. "?INH{{C (HOE’50IJI 9.**OIHV Patent Application Publication Apr. 28, 2016 Sheet 5 of 10 US 2016/O115499 A1 ºsoionsaso?onaeasoon?º Patent Application Publication Apr. 28, 2016 Sheet 6 of 10 US 2016/O115499 A1 s Patent Application Publication Apr. 28, 2016 Sheet 7 of 10 US 2016/O115499 A1 1218 bp B 2O,O% 100.0% 3O,O% 60.0% 40.0% 20.0% O.0% WT sci231, sci231, sci?32, Sci232, if1 fi2 ifi if2 FIG.SB Patent Application Publication Apr. 28, 2016 Sheet 8 of 10 US 2016/O115499 A1 FIG. 6A FIG. 6C FIG. 6B FIG. 6D Patent Application Publication Apr. 28, 2016 Sheet 9 of 10 US 2016/O115499 A1 FIG. 7A FIG. 7B Patent Application Publication Apr. 28, 2016 Sheet 10 of 10 US 2016/O115499 A1 S$8.3 gets S8. 8:3, 3 g88s 3.33 targets 33 3. lists contai: 2838 unique xiernets F.G. 8 US 2016/01 15499 A1 Apr. 28, 2016 MATERALS AND METHODS FOR have failed (Taniguchi et al. (2008)), suggesting that the CONTROLLING BUNDLE SHEATH CELL mesophyll and bundle sheath cells must be engineered sepa FATE AND FUNCTION IN PLANTS rately (Kajala et al. (2011)). 0005. Despite the pivotal role ofbundle sheath cells in C4 CROSS-REFERENCE TO RELATED photosynthesis, the mechanisms that determine their cell APPLICATION identity and patterning are still unknown. Extensive mutant screening efforts in the past decades have identified several 0001. The present application claims the benefit of U.S. maize and Arabidopsis mutants defective in chloroplast Provisional Application No. 61/833,771, filed Jun. 11, 2013, development in the bundle sheath cells (Nelson (2011); Brut which is hereby incorporated by reference herein in its nell et al. (1999); Hall et al. (1998); Kinsman and Pyke entirety, including any figures, tables, nucleic acid sequences, (1998); Petricka et al. (2008); Rossinietal. (2001)), but none amino acid sequences, or drawings. of these mutants affects bundle sheath cell identity. 0006 Bundle sheath cells are a leaf cell type that forms a BACKGROUND OF THE INVENTION single cell layer between the mesophyll cells and the central 0002 With a rapidly growing world population and dwin vascular tissue. In C3 plants, both the mesophyll cells and BS dling natural resources, we are facing an enormous challenge cells are photosynthetic, but the BS cells are small with fewer of increasing crop yields while simultaneously improving the chloroplasts. In contrast, the BS cells are the major sites of efficiency of resource utilization. In C3 plants, a 3-carbon photosynthesis in most C4 plants, whereas the mesophyll molecule is the first product of carbon fixation, whereas in C4 cells are involved in CO, fixation only. Accordingly, the BS plants, a 4-carbon molecule is the first product. Because C4 cells are much larger in size. The spatial separation of the two plants are much more efficient than C3 plants in photosyn phases of photosynthesis into mesophyll and BS cells is one thesis as well as water and nitrogen usage, particularly in hot of the features that make C4 plants significantly more effi climates (Langdale (2011)), tremendous efforts are being cient photosynthetically. Another feature that improves the taken to introduce C4 photosynthesis into economically photosynthetic efficiency in C4 plants is the Kranzanatomy, important C3 crops (Sage and Zhu (2011)), such as rice characterized by an approximately 1:1 ratio between meso (Hibberd et al. (2008)). It is estimated that yields can be phyll and BS cells. The close association between the two cell increased by 50% if rice is transformed into a C4 plant (Hib types facilitates metabolite transport, which is critical for the berdet al. (2008)). C4 mechanism. In C3 plants, this ratio is greater than 2:1. 0003) Evidence indicates that C4 plants have evolved mul 0007 Many important crops, such as rice (Oryza sativa) tiple times from C3 plants (Brown et al. (2011)), but all C4 and wheat (Triticum aestivum), are C3 plants. To meet the plants share some common features that make them perform needs for food of a rapidly growing population, tremendous better. A critical innovation is the deployment of phospho efforts are being undertaken to introduce the C4 mechanism enolpyruvate (PEP) carboxylase as the enzyme for the initial into C3 crops (Langdale, 2011). For example, millions of fixation of CO, in C4 plants. Unlike RUBISCO, the enzyme dollars have been invested at the C4 rice consortium to con used for the initial fixation of CO in C3 plants, PEP carboxy Vert this important crop into a C4 plant (von Caemmereret al., lase does not have an oxygenase activity and therefore can 2012). Although the input is huge and the risk is high, the maintain a high rate of photosynthesis even under conditions potential reward is enormous. It is estimated that a 10% of low CO (stomates partially closed) and high temperature increase in the photosynthetic efficiency would increase the (RUBISCO’s oxygenase activity is stimulated at high tem yield by 50% (Langdale, 2011). However, to achieve C4 peratures (Spreitzer et al. (2002)). Another critical feature of photosynthesis in C3 plants requires engineering of the BS C4 plants is the separation of the two phases of photosynthe and mesophyll cells at many levels, including an increase in sis, namely CO fixation and carbohydrate biosynthesis, into the density of BS cells and modification of the physiology in the mesophyll and bundle sheath cells, respectively. To sus the BS and mesophyll cells. This in turn demands a good tain a high rate of photosynthesis, C4 plants also have numer understanding of the mechanisms that control BS and meso ous plasmodesmata and various types of nutrient transporters phyll cell fate. However, at present, the molecular basis of BS distributed along the cell wall between the mesophyll and cell-fate specification is still unclear (Nelson, 2011). bundle sheath cells (Haritatos et al. (2000); Takahashi et al. 0008. There is evidence that the development of BS cells is (2000)), which ensure efficient transport of the primary prod determined by a signal from the vascular tissue (Langdale et ucts from the CO fixation process. In the bundle sheath cells, al., 1988: Langdale et al., 1991; Jankovsky et al., 2001), but CO is released from the primary photosynthetic product and nothing is known about the nature of this positional informa is then utilized in a standard C3-type photosynthesis involv tion. Although several factors with a role in chloroplast devel ing RUBISCO. RUBISCO is expressed only in the bundle opment in BS cells have been reported, none of these appears sheath cells, whereas PEP carboxylase is mesophyll cell spe to control BS cell fate. In maize (Zea mays), for example, cific. Due to the spatial separation of the photosynthetic pro mutations in the genes encoding GOLDEN2 and related tran cesses along with the active transport system, CO is effec scription factors (Hall et al., 1998; Rossini et al., 2001), as tively concentrated in the bundle sheath cells, which in turn well as BSD2 (BUNDLE SHEATH DEFECTIVE2), a DnaJ leads to the repression of the oxygenase activity of like protein (Brutnell et al., 1999), disrupt chloroplast devel RUBISCO.
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  • Oscaf2 Contains Two CRM Domains and Is Necessary for Chloroplast
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