Bioengineering and Management for Efficient Phosphorus Utilization In

中国COBIOT-1045;科技论文在线 NO. OF PAGES 6 http://www.paper.edu.cn

Available online at www.sciencedirect.com

Bioengineering and management for efﬁcient phosphorus

utilization in crops and pastures

1 1 2 3 1

Jiang Tian , Xiurong Wang , Yiping Tong , Xinping Chen and Hong Liao

Phosphorus (P) is one of the three macronutrients for plants. critical to develop ‘smart’ crop cultivars with high P

Because of its low mobility and high fixation in soils, low P efficiency (PE), defined as the ability to grow and yield

availability is a worldwide constraint for crop productivity. in soils with reduced P availability [4]. Sustainable

Molecular biology provides great opportunities to improve P increases in crop yield with efﬁcient utilization of irre-

efﬁciency in plants. However, transgenic plants cannot be placeable P resources will entail better management and

commercialized before integrating all the knowledge on development of cultivars with high P efﬁciency.

bottlenecks for improving P efﬁciency of crops/pastures. This

review intends to summarize the main strategies of With the development of biotechnology, more and more

bioengineering to improve P efﬁciency of crops/pastures, biotech crops have been commercialized and their plant-

including conventional and molecular assisted breeding, ing areas have dramatically increased from 1.7 to 148

identiﬁcation and application of key genes for biotech plants. It million hectares between 1996 and 2010, which stands in

highlights recent advances in the understanding of improving P contrast to the nearly constant total area of crops

efﬁciency through the integration of bioengineering with P (Figure 1), showing the increasing contribution of biotech

fertilization and cultivation management. crops to modern agriculture. However, most commercia-

Addresses lized biotech crops are developed to resist insects and/or

State Key Laboratory for Conservation and Utilization of Subtropical herbicides. Little progress has been made for nutrient

Agro-bioresources, Root Biology Center, South China Agricultural efﬁciency, especially for PE due to its complexity. Here,

University, Guangzhou 510642, China

2 we highlight the recent progress on facilitating P utiliz-

State Key Laboratory for Plant Cell and Chromosome Engineering,

ation in crops/pastures through conventional and molecu-

Institute of Genetics and Developmental Biology, Chinese Academy of

Sciences, Beijing 100101, China lar assisted breeding, biotechnology, P fertilization, and

Department of Plant Nutrition, China Agricultural University, Beijing, cultivation management.

100193, China

Corresponding author: Liao, Hong ([email protected]) Improving P efﬁciency via conventional and

marker assisted selection breeding

It is well documented that genetic variations for PE exist

Current Opinion in Biotechnology 2012, 23:1–6

among plant species and genotypes within a species,

This review comes from a themed issue on indicating that it is possible to improve plant PE through

Phosphorous Biotechnology conventional and marker assisted selection (MAS) breed-

Edited by Lars Blank and Andrew Shilton

ing. MAS is a process using markers (morphological,

biochemical or one based on DNA/RNA variation) to

select the traits of interest during breeding. Root traits

0958-1669/$ – see front matter

are thought to be crucial for P uptake. This ‘root breed-

ing’ strategy has proven effective in improving PE of

some crops (e.g. soybean) [5]. In order to overcome

DOI 10.1016/j.copbio.2012.03.002

limitations of genetic variations within the same species,

transferring alien genes from other species even pastures

Introduction to crops through chromosome engineering is an effective

It is always a critical challenge for the agricultural sector to approach in improving PE of crops. For example, wheat

feed the increasing population. In recent years, world lines carrying 1BL/1RS, 1AL/1RS or 1DL/1RS wheat–rye

primary crop area has held steady due to the shortage of chromosomal translocations (the long arm of wheat

arable land reserves (Figure 1). Therefore, the annual chromosomes 1A, 1B, and 1D is replaced by the short

consumption of global chemical fertilizers has to be arm of rye chromosome 1R, respectively) exhibited

increased to meet the huge demands for food. Since increased PE and higher yield [6]. However, the root

phosphorus (P) fertilizer is mainly produced from dwind- traits associated with PE are hidden in soils, therefore root

ling supplies of the non-renewable resource, phosphate breeding through conventional phenotype selection is

(Pi) rock [1,2], increased consumption of P fertilizers time consuming and complicated. MAS breeding might

cannot keep pace with increased utilization of total be better as demonstrated by recent achievements in rice

chemical fertilizers (Figure 1). Furthermore, due to its [7 ]. Through the major quantitative trait locus (QTL)

low mobility and high ﬁxation in soils, low P availability is controlling P uptake, phosphorus uptake1 (Pup1), improved

a worldwide constraint for crop growth [3]. Therefore, it is PE and yield of rice genotypes have been successfully

www.sciencedirect.com Current Opinion in Biotechnology 2012, 23:1–6

Please cite this article in press as: Tian J, et al.. Bioengineering and management for efﬁcient phosphorus utilization in crops and pastures, Curr Opin Biotechnol (2012), doi:10.1016/ j.copbio.2012.03.002 转载

中国科技论文在线 http://www.paper.edu.cn

COBIOT-1045; NO. OF PAGES 6

2 Phosphorous Biotechnology

Figure 1

1500 180

Primary crop Total fertilzers

Biotec h crop P fertilizer 170 1400 160 1300 150 1200 140

1100 130 200 50

40 150 30

Crop area (million hectares) Crop area (million 100 20 Fertilizer consumption (million tons) consumption (million Fertilizer 50 10

0 0 1996 1998 2000 2002 2004 2006 2008 2010 Year

Current Opinion in Biotechnology

World primary crop and biotech crop planting area, along with global annual consumption of total chemical fertilizers and P fertilizer over the period

from 1996 to 2010. World primary crop area was the total planting area of main crops. The total chemical fertilizers were the sum of fertilizer N, P and K.

(Data of GM crops are from http://www.isaaa.org/resources/publications/pocketk/16/default.asp. The other data are from FAOSTAT [http://

faostat.fao.org/], accessed January 10, 2012).

developed. However, most identiﬁed QTLs made small regulation of root hair development and enhanced gly-

contributions to PE, and thus were impractical for MAS cerophosphodiester turnover [13]. Many other genes have

breeding [8,9]. been identiﬁed to mediate root architectural changes in

crops and pastures, such as crown rootless 5 (OsCRL5) and

Improving P efﬁciency via transgenic expansin 17 (OsEXPA17) in rice [14,15 ], but they need to

modiﬁcation be tested for any contributions to improving PE. There-

Plants have evolved multiple adaptations to low P avail- fore, while progress has been realized, improving PE

ability for efﬁcient utilization of P from soils. Under- through transgenic modiﬁcation of root architecture has

standing the mechanisms and identifying genes involved a long way to go.

in these adaptations promises to facilitate improvement of

PE in crops and pastures through transgenic modiﬁcation. Releasing Pi from insoluble P pools in rhizosphere

Since over 99% of soil P exists as poorly available forms to

Optimizing root architecture for Pi acquisition plants [16], an important trait for optimal PE complemen-

Because of the immobility and heterogeneous distri- tary to the development of optimal root architecture is the

bution of Pi in soils, root architecture traits that establish ability to stimulate release of Pi from insoluble P pools in

the framework of root system and enhance topsoil fora- the rhizosphere. It has been well documented that

ging are particularly important for Pi acquisition secreted protons (H ), organic acids (OAs) and phospha-

(Figure 2) [4]. The architectural traits mainly include tases play vital roles for plants to mobilize and utilize the

shallower root angles, enhanced adventitious rooting and ﬁxed P in soils (Figure 2).

lateral root branching, greater root hair density, and more

+ +

cluster root formation [4,10,11]. However, the underlying Since H -ATPases mediate ATP-dependent H extru-

molecular mechanisms of root architecture adaptation to sion to the extracellular space, the genes affecting

+ +

P deﬁciency remain unclear [4,5]. Recently, a b-expansin H -ATPases should be crucial for H secretion from roots,

gene, GmEXPB2 from soybean was shown to be critical as well as subsequent P acquisition. In support of this,

for regulating root architecture responses to Pi starvation knockout of OsA8, a P-type H -ATPase gene, which

in crops, and overexpressing GmEXPB2 could success- affected transcripts of several other H -ATPases, inhibited

fully improve PE in soybean [12 ]. In pasture plants, P acquisition in rice mutants [17].

two glycerophosphodiester phosphodiesterase genes, LaGPX-

PDE1 and LaGPX-PDE2 from white lupin, were reported It is generally assumed that secreted OAs could mobilize

to participate in acclimation to P deﬁciency through the insoluble P through both rhizosphere acidiﬁcation and

Current Opinion in Biotechnology 2012, 23:1–6 www.sciencedirect.com

中国科技论文在线 http://www.paper.edu.cn

COBIOT-1045; NO. OF PAGES 6

Bioengineering and management for efficient phosphorus utilization Tian et al. 3

Figure 2

1. Optimizing root architecture for Pi acquisition

(GmEXPB2, LaGPX-PDE1,LaGPX-PDE2)

Pi 2. Releasing Pi from insoluble P pools

(OsA8 , PoMDH, TaALMT1, PvPAP3)

Pht1 3. Enhancing expression of high affinity Pi PHR1

SPX1 transporter (OsP ht1:2,OsPht1:8)

Pi 4. Modifyin g regulators in P signaling network

PTF1

Ca-P (OsPTF1 ,OsPHR2,OsSPX1,ath-miR399d) H+

Fe-P ATPase

EXPB2 EXPB2

Al-P Malate Organic P (Phytate, ATP) APase MT1 MDH, CS CS MDH, Pi Pi

Pi Pi Pht1 Pht1

Current Opinion in Biotechnology

A model for improved P efficiency in crops and pastures through transgenic engineering. The genes in parenthesis have been used in transgenic

modification for improving P efficiency in crops, pastures. The first two letters of the gene label represent the abbreviated species name, except ath-

miR399d from Arabidopsis. Os: Oryza sativa; La: Lupinus albus; Po: Penicillium oxalicum; Ta: Triticum aestivum; Pv: Phaseolus vulgaris.

chelation of metal ions, and that this process is mainly enhance phytate-P utilization in crops and pasture plants

determined by activities of OA transporters and enzymes through genetic modiﬁcation.

for OA metabolism, such as phosphoenolpyruvate

carboxylase (PEPC), malate dehydrogenase (MDH), Enhancing expression of high afﬁnity Pi transporter

and citrate synthase (CS) [18]. A number of reports Phosphate acquisition and translocation in plants are

provided support for OA roles in improved P acquisition mediated by Pi transporters (PT). Among them, members

from insoluble sources through overexpression of OA from the high afﬁnity PT family, Pht1, mainly function in

related genes, such as PoMDH from Penicillium oxalicum Pi acquisition from soils and translocation from roots to

in tobacco and aluminum activated malate transporter1 from other parts of plants [28]. Although overexpressing

Triticum aestivum (TaALMT1) in barley [19,20]. These NtPht1;1, OsPht1;2 or OsPht1;8 facilitated Pi acquisition

results indicated that some OA-related genes might be in transgenic rice plants, their biomass and yield were not

useful for biotech improvement of PE. coincidently improved due to the toxicity of excess P at

high P level [29–31], suggesting that overexpressing Pht1

Organic P often accounts for 30–70% of total soil P, which in crops should be integrated with soil/farm management

is not directly available to plants unless hydrolyzed by in order to improve crop PE (Figure 2).

phosphatases [21]. Enhanced exudation and activities of

phosphatases, therefore, become potential hotspots for Modifying regulators in P signaling network

improving PE through genetic engineering. It has been Plant responses to P deﬁciency are coordinately regulated

documented that overexpressing the purple acid phospha- by an elaborate signaling network involving many actors,

tase 3, PvPAP3 in bean results in increased utilization of including phytohormones, sugars, miRNAs, transcription

extracellular ATP [22 ]. In addition, another class of factors, and other regulators [32 ]. Among these partici-

enzymes, phytases from microorganisms and plants has pants, miRNAs, SPX (SYG/PHO81/XPR1) domain con-

been used to improve phytate-P utilization in crops and taining proteins, and several transcription factors are

pasture plants. Instances of this strategy include over- major components for regulating P homeostasis in plants

expression of a phytase gene, phyA from Aspergillus niger in [33]. Interestingly, overexpression of a transcription fac-

cotton [23], EcappA from Escherichia coli in potato [24], tor, PTF1 (Pi starvation induced transcription factor 1),

AtPAP15 from Arabidopsis in soybean [25 ], MtPHY1 and enhanced PE in both rice and maize [34,35 ]

MtPAP1 from Medicago truncatula in clover [26], and (Figure 2). Conversely, overexpressing a transcription

LASAP2 from white lupin in tobacco [27], suggesting factor, phosphate starvation response 2 (OsPHR2), a major

that increased activities of root secreted phytases could component in P signaling pathways in rice, resulted in

www.sciencedirect.com Current Opinion in Biotechnology 2012, 23:1–6

中国科技论文在线 http://www.paper.edu.cn

COBIOT-1045; NO. OF PAGES 6

4 Phosphorous Biotechnology

increased P concentration but inhibited plant growth, and lack of genetic variability severely inhibit wide

which might be caused by excessive P amounts in leaves application of conventional and MAS breeding to improve

[36]. Similar results were also observed in modifying SPX PE. Although these problems could be solved using

and miR399. Suppressing OsSPX1 in rice, and overex- genetic engineering techniques, selecting the suitable

pressing ath-miR399d from Arabidopsis in tomato led to candidate genes is a big challenge, and also the suitable

excessive P accumulation in leaves, and subsequently candidate genes might be variety or species dependent.

inhibited plant growth [37 ,38]. Therefore, improving PE Additionally, P fertilization management could affect

through transforming the critical genes in P signaling dynamics of rhizosphere P, and subsequently affect P

networks requires more insights into the physiological acquisition efﬁciency in plants. Moreover, competition

and molecular connections between components. might also inﬂuence the P uptake of intercropped species.

Therefore, more intensive studies are required to further

Improving P efﬁciency via better P fertilization elucidate the critical procedures mediating superior PE in

and cultivation management plants and P fertilization as well as cultivation manage-

To feed the increasing population, large-scale fertiliza- ment in the ﬁeld.

tion and excessive consumption of natural P resources are

increasing, and thus result in severe environmental pro- In conclusion, through integration of breeding, genetic

blems [39]. Improving P utilization only from the plant engineering, P fertilization and cultivation management,

side is not enough to optimize P utilization and solve the optimum PE and productivity of crops/pastures can be

environmental problems caused by soil P accumulation. synchronously achieved with the better understanding of

For this, soil-testing based upon ‘building-up and main- plants, soils and management.

tenance’ was developed and widely used in developed

countries and some fast developing countries (e.g. China) Acknowledgements

The authors acknowledge Dr Thomas Walk for critical reading, Dr Xing Lu

[40]. The principle of this approach is to adjust soil P

for preparing Figure 1, and ﬁnancial supports from the National Natural

levels from those threatening environmental damage or P

Science Foundation of China (Grant Nos. 30890130 and 31025022) and

deﬁciency to the levels ensuring stable crop yield. This National Key Basic Research Special Funds of China (2011CB100301).

method is particularly useful for controlling high soil P

accumulation and reducing environmental risks. The References and recommended reading

Papers of particular interest, published within the period of review,

rhizosphere-based P management is an alternative

have been highlighted as:

approach to improve PE and crop yield through exploita-

tion of biological potentials for efﬁcient mobilization and of special interest

of outstanding interest

acquisition of P by crops, and reducing the overreliance

on application of chemical fertilizer P [41]. The match

1. Cordell D, Drangert J, White S: The story of phosphorus: global

between demand and supply can be strongly improved by

food security and food for thought. Global Environ Change 2009,

positioning mineral fertilizers close to the expanding root 19:292-305.

system [42], and thus rhizosphere-based P management is

2. Beardsley TM: Peak phosphorus. BioScience 2011, 61:91.

a priority for improving P fertilizer use efﬁciency.

3. Sa´ nchez-Caldero´ n L, Chacon-Lo´ pez A, Pe´ rez-Torres CA, Herrera-

Estrella L: Phosphorus: plant strategies to cope with its

scarcity. Plant Cell Monogr 2010, 17:173-198.

Soil P exists in various forms that require different bio-

chemical or chemical reactions to release Pi. It is well 4. Lynch JP: Root phenes for enhanced soil exploration and

phosphorus acquisition: tools for future crops. Plant Physiol

known that plant species vary in utilization of different

2011, 156:1041-1049.

P forms, and this kind of biodiversity can be applied to

5. Wang X, Yan X, Liao H: Genetic improvement for phosphorus

improve PE of crops/pastures through cultivation man-

efﬁciency in soybean: a radical approach. Ann Bot 2010,

agement, such as intercropping. Complementarity can 106:215-222.

occur within intercropped species for different soil P pools.

6. Ehdaie B, Merhaut DJ, Ahmadian S, Hoops AC, Khuong T,

Legumes generally have higher capacities to mobilize soil Layne AP, Waines JG: Root system size inﬂuences water-

nutrient uptake and nitrate leaching potential in wheat. J Agron

Pi than cereals [43], and thus are successfully used to

Crop Sci 2010, 196:455-466.

improve Pi uptake and yield of cereal crops grown on P

7. Chin JH, Gamuyao R, Dalid C, Bustamam M, Prasetiyono J,

deﬁcient soils through legume–cereal intercropping

Moeljopawiro S, Wissuwa M, Heuer S: Developing rice with high

[43,44 ]. The cultivation management can also be used yield under phosphorus deﬁciency: Pup1 sequence to

application. Plant Physiol 2011, 156:1202-1216.

to improve the productivity and sustainability of pasture-

This paper deﬁnes a core set of Pup1 markers, and identiﬁes sequence

land which often receives low or no input of fertilizers. polymorphisms suitable for single nucleotide polymorphism marker

development for high-throughput genotyping. Furthermore, using a mar-

ker-assisted backcrossing approach, Pup1 was introgressed into differ-

Perspectives ent rice varieties. These results suggest that Pup1 is effective in different

genetic backgrounds and environments and that it has the potential to

Some progress has been made to improve PE in crops and

signiﬁcantly enhance grain yield under ﬁeld conditions.

pasture plants mainly through the three strategies dis-

8. Liang Q, Cheng XH, Mei MT, Yan XL, Liao H: QTL analysis of root

cussed in this review. However, any individual strategy

traits as related to phosphorus efﬁciency in soybean. Ann Bot

might have disadvantages. For example, incompatibility 2010, 106:223-234.

Current Opinion in Biotechnology 2012, 23:1–6 www.sciencedirect.com

中国科技论文在线 http://www.paper.edu.cn

COBIOT-1045; NO. OF PAGES 6

Bioengineering and management for efficient phosphorus utilization Tian et al. 5

9. Ren YZ, He X, Liu DC, Li JJ, Zhao XQ, Li B, Tong YP, Zhang AM, 23. Liu J, Zhao C, Ma J, Zhang G, Li M, Yan G, Wang X, Ma Z:

Li ZS: Major quantitative trait loci for seminal root morphology Agrobacterium-mediated transformation of cotton

of wheat seedlings. Mol Breeding 2011 doi: 10.1007/s11032- (Gossypium hirsutum L.) with a fungal phytase gene improves

011-9605-7. phosphorus acquisition. Euphytica 2011, 181:31-40.

10. Hill JO, Simpson RJ, Ryan MH, Chapman DF: Root hair 24. Hong Y, Liu C, Cheng K, Hour A, Chan M, Tseng T, Chen K,

morphology and mycorrhizal colonisation of pasture species Shaw J, Yu S: The sweet potato sporamin promoter confers

in response to phosphorus and nitrogen nutrition. Crop Pasture high level phytase expression and improves organic

Sci 2010, 61:122-131. phosphorus acquisition and tuber yield of transgenic potato.

Plant Mol Biol 2008, 67:347-361.

11. Lambers H, Finnegan PM, Laliberte´ E, Pearse SJ, Ryan MH,

Shane MW, Veneklaas EJ: Phosphorus nutrition of proteaceae 25. Wang X, Wang Y, Tian J, Lim B, Yan X, Liao H: Overexpressing

in severely phosphorus-impoverished soils: are there lessons AtPAP15 enhances phosphorus efﬁciency in soybean. Plant

to be learned for future crops? Plant Physiol 2011, Physiol 2009, 151:233-240.

156:1058-1066. This study demonstrates that increased P acquisition and yield was

observed in transgenic soybean plants with overexpressing an Arabi-

12. Guo WB, Zhao J, Qin L, Yan XL, Liao H: A soybean b-Expansin

dopsis purple acid phosphatase (AtAPA15) containing a carrot extra-

gene GmEXPB2 intrinsically involved in root system

cellular targeting peptide. This is the ﬁrst report on the improvement of P

architecture responses to abiotic stresses. Plant J 2011,

efﬁciency in soybean through constitutive expression of a plant acid 66:541-552.

phosphatase gene.

In this work, a phosphate starvation-induced vegetative b-expansin gene,

GmEXPB2, was cloned. Furthermore, it demonstrates that GmEXPB2 26. Ma X, Wright E, Ge Y, Bell J, Xi Y, Bouton J, Wang Z: Improving

may enhance both P efﬁciency and P responsiveness by regulating phosphorus acquisition of white clover (Trifolium repens L.) by

adaptive changes of the root system architecture. This ﬁnding has great transgenic expression of plant derived phytase and acid

agricultural potential for improving crop P uptake on both low-P and P- phosphatase genes. Plant Sci 2009, 176:479-488.

fertilized soils.

27. Wasaki J, Maruyama H, Tanaka M, Yamamura T, Dateki H,

13. Cheng L, Bucciarelli B, Shen J, Allan D, Vance C: Update on white Shinano T, Ito S, Osaki M: Overexpression of the LASAP2 gene

lupin cluster root acclimation to phosphorus deﬁciency. Plant for secretory acid phosphatase in white lupin improves the

Physiol 2011, 156:1025-1032. phosphorus uptake and growth of tobacco plants. Soil Sci

Plant Nutri 2009, 55:107-113.

14. Kitomi Y, Ito H, Tokunori H, Koichiro A, Hidemi K, Yoshiaki I: The

auxin responsive AP2/ERF transcription factor CROWN 28. Bucher M: Functional biology of plant phosphate uptake at root

ROOTLESS5 is involved in crown root initiation in rice through and mycorrhiza interfaces. New Phytol 2007, 173:11-26.

the induction of OsRR1, a type-A response regulator of

29. Liu F, Wang Z, Ren H, Shen C, Li Y, Ling H, Wu C, Lian X, Wu P:

cytokinin signaling. Plant J 2011, 67:472-484.

OsSPX1 suppresses the function of OsPHR2 in the regulation

15. Yu Z, Kang B, He X, Lv S, Bai Y, Ding W, Chen M, Cho H, Ping W: of expression of OsPT2 and phosphate homeostasis in shoots

Root hair-speciﬁc expansins modulate root hair elongation in of rice. Plant J 2010, 62:508-517.

rice. Plant J 2011, 66:725-734.

30. Park MR, Tyagi K, Baek SH, Kim YJ, Rehman S, Yun SJ:

This study demonstrates that a root hair-speciﬁc expansin, OsEXPA17

Agronomic characteristics of transgenic rice with enhanced

was identiﬁed from a rice mutant with short root hairs, which is required

phosphate uptake ability by overexpressed tobacco high

for root hair elongation. These results suggest that members of the root

afﬁnity phosphate transporter. Pak J Bot 2010, 42:3265-3273.

hair EXPA subclade play a crucial role in root hair cell elongation in

Graminaceae.

31. Jia H, Ren H, Gu M, Zhao J, Sun S, Zhang X, Chen J, Wu P,

The phosphate transporter gene OsPht1;8 is involved

16. Hesterberg D: Macroscale chemical properties and X-ray Xu G:

in phosphate homeostasis in rice

absorption spectroscopy of soil phosphorus. In Developments . Plant Physiol 2011,

156

in Soil Science, vol. 34. Edited by Singh B, Grafe M. Elsevier; :1164-1175.

2010:313-356.

32. Chiou TJ, Lin SI: Signaling network in sensing phosphate

availability in plants. Annu Rev Plant Biol 2011, 62:185-206.

17. Chang C, Hu Y, Sun S, Zhu Y, Ma G, Xu G: Proton pump OsA8 is In this work, the authors integrate and discuss the present knowledge of

linked to phosphorus uptake and translocation in rice. J Exp the molecular mechanisms and networks with regard to phosphate

Bot 2009, 60:557-565. sensing and signaling in plants.

18. Plaxton WC, Tran HT: Metabolic adaptations of phosphate- 33. Caldero´ n-Va´ zquez C, Sawers RJH, Herrera-Estrella L: Phosphate

starved plants. Plant Physiol 2011, 156:1006-1015. deprivation in maize: genetics and genomics. Plant Physiol

2011, 156:1067-1077.

19. Delhaize E, Taylor P, Hocking PJ, Simpson RJ, Ryan PR,

Richardson AE: Transgenic barley (Hordeum vulgare L.) 34. Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P: OsPTF1, a novel

expressing the wheat aluminum resistance gene (TaALMT1) transcription factor involved in tolerance to phosphate

shows enhanced phosphorus nutrition and grain production starvation in rice. Plant Physiol 2005, 138:2087-2096.

when grown on an acid soil. Plant Biotechnol J 2009, 7:391-400.

35. Li Z, Gao Q, Liu Y, He C, Zhang X, Zhang J: Overexpression of

20. Lu¨ J, Gao X, Dong Z, Yi J, An L: Improved phosphorus transcription factor ZmPTF1 improves low phosphate

acquisition by tobacco through transgenic expression of tolerance of maize by regulating carbon metabolism and root

mitochondrial malate dehydrogenase from Penicillium growth. Planta 2011, 233:1129-1143.

oxalicum. Plant Cell Rep 2011 doi: 10.1007/s00299-011-1138-3. This work shows that a phosphate starvation responsive transcription

factor, ZmPTF1 was cloned from maize. Furthermore, overexpressing

21. Vincent AG, Schleucher J, Gro¨ bner G, Vestergren J, Persson P,

ZmPTF1 improves phosphate efﬁciency of maize through regulating

Jansson M, Giesler R: Changes in organic phosphorus

carbon metabolism and root growth. This research provides a useful

composition in boreal forest humus soils: the role of iron and

gene for transgenic breeding of maize with superior phosphorus efﬁ-

aluminum. Biogeochemistry 2011 doi: 10.1007/s10533-011- ciency.

9612-0.

36. Zhou J, Jiao F, Wu Z, Wang X, He X, Zhong W, Wu P: OsPHR2 is

22. Liang CY, Tian J, Lam HM, Lim BL, Yan XL, Liao H: Biochemical

involved in phosphate-starvation signaling and excessive

and molecular characterization of PvPAP3, a novel purple acid

phosphate accumulation in shoots of plants. Plant Physiol

phosphatase isolated from common bean enhancing

2008, 146:1673-1686.

extracellular ATP utilization. Plant Physiol 2010, 152:854-865.

In this study, a novel purple acid phosphatase (PAP), PvPAP3, was 37. Wang C, Ying S, Huang H, Li K, Wu P, Shou H: Involvement of

puriﬁed in bean. Furthermore, overexpressing PvPAP3 enhanced root OsSPX1 in phosphate homeostasis in rice. Plant J 2009,

growth and P uptake when ATP was supplied as the sole external P 57:895-904.

source. These results suggest that PvPAP3 might function in the adapta- In the study, suppression of OsSPX1 resulted in over-accumulation of

tion of bean to P deﬁciency, possibly through enhancing utilization of phosphate in rice. However, overexpression of OsSPX1 suppressed

extracellular ATP as a P source. expression levels of 10 phosphate starvation-induced genes in rice.

www.sciencedirect.com Current Opinion in Biotechnology 2012, 23:1–6

中国科技论文在线 http://www.paper.edu.cn

COBIOT-1045; NO. OF PAGES 6

6 Phosphorous Biotechnology

These results suggest that OsSPX1 acts via a negative feedback loop to 42. Jing J, Rui Y, Zhang F, Rengel Z, Shen J: Localized application

optimize growth under phosphate-limited conditions. of phosphorus and ammonium improves growth of

maize seedlings by stimulating root proliferation and

38. Gao N, Su Y, Min J, Shen W, Shi W: Transgenic tomato

rhizosphere acidiﬁcation. Field Crops Res 2010,

overexpressing ath-miR399d has enhanced phosphorus 119:355-364.

accumulation through increased acid phosphatase and

proton secretion as well as phosphate transporters. Plant Soil 43. Hinsinger P, Betencourt E, Bernard L, Brauman A, Plassard C,

2010, 334:123-136. Shen J, Tang X, Zhang F: P for two, sharing a scarce resources:

soil phosphorus acquisition in the rhizosphere of intercropped

39. Domagalski J, Lin C, Luo Y, Kang J, Wang S, Brown LR, Munn MD:

species. Plant Physiol 2011, 156:1078-1086.

Eutrophication study at the Panjiakou-Daheiting Reservoir

system, northern Hebei Province, People’s Republic of China:

44. Fang S, Gao X, Deng Y, Chen X, Liao H: Crop root behavior

Chlorophyll-a model and sources of phosphorus and nitrogen.

coordinates phosphorus status and neighbors: from ﬁeld

Agric Water Manage 2007, 94:43-45.

studies to three-dimensional in situ reconstruction of root

system architecture. Plant Physiol 2011, 155:1277-1285.

40. Li H, Huang G, Meng Q, Ma L, Yuan L, Wang F, Zhang W, Cui Z,

In this work, plant growth responses to phosphorus stress of two maize

Chen X, Shen X, Jiang R, Zhang F: Integrated soil and plant

varieties intercropped with soybean were examined in the ﬁeld and in a

phosphorus management for crop and environmental in

transparent gel system. Results showed that plant roots could integrate

China. A review. Plant Soil 2011, 349:157-167.

information on phosphorus status and root behavior of neighboring

plants. This study provides new insights into the dynamics and complex-

41. Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, Zhang W, Zhang F:

ity of root behavior and kin recognition among crop species in response to

Phosphorus dynamics: from soil to plant. Plant Physiol 2011,

156:997-1005. nutrient status and neighboring plants.

Current Opinion in Biotechnology 2012, 23:1–6 www.sciencedirect.com