Total RNA was extracted from three Arabidopsis seedlings per pot
using RNAiso Plus (Takara Bio, Japan) according to the manufacturer’s
instructions. Three biological replicates per treatment were performed
for RNA-Seq analysis. The extracted RNA was used to construct
paired-end libraries using a TruSeq Stranded mRNA Sample Prep
Kit (Illumina). The libraries were sequenced on an Illumina
NovaSeq6000 sequencer with a 151-bp paired-end protocol (Macrogen). Trimmomatic v0.3964 with the options SLIDINGWINDOW:4:20
and MINLEN:40 was used for trimming low-quality reads and adaptor
sequences. Trimmed reads were mapped against the reference
sequence of TAIR10 (https://www.arabidopsis.org/) using STAR v2.5.165
with the options outSAMstrandField: intronMotif; and outFilterType:
1.
Nature Communications | (2023)14:5047
2.
3.
4.
5.
Pennisi, E. The blue revolution, drop by drop, gene by gene. Science
320, 171–173 (2008).
Fujita, Y., Fujita, M., Shinozaki, K. & Yamaguchi-Shinozaki, K. ABAmediated transcriptional regulation in response to osmotic stress in
plants. J. Plant Res. 124, 509–525 (2011).
Zhang, H., Zhu, J., Gong, Z. & Zhu, J. K. Abiotic stress responses in
plants. Nat. Rev. Genet. 23, 104–119 (2022).
Skirycz, A. et al. Survival and growth of Arabidopsis plants given
limited water are not equal. Nat. Biotechnol. 29, 212–214 (2011).
Claeys, H., Van Landeghem, S., Dubois, M., Maleux, K. & Inzé, D.
What is stress? Dose-response effects in commonly used in vitro
stress assays. Plant Physiol. 165, 519–527 (2014).
13
Article
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
Verslues, P. E. Time to grow: factors that control plant growth
during mild to moderate drought stress. Plant Cell Environ. 40,
177–179 (2017).
Harb, A., Krishnan, A., Ambavaram, M. M. R. & Pereira, A. Molecular
and physiological analysis of drought stress in Arabidopsis reveals
early responses leading to acclimation in plant growth. Plant Physiol. 154, 1254–1271 (2010).
Des Marais, D. L. et al. Physiological genomics of response to soil
drying in diverse Arabidopsis accessions. Plant Cell 24,
893–914 (2012).
Ma, X., Sukiran, N. L., Ma, H. & Su, Z. Moderate drought causes
dramatic floral transcriptomic reprogramming to ensure successful
reproductive development in Arabidopsis. BMC Plant Biol. 14, 164
(2014).
Clauw, P. et al. Leaf growth response to mild drought: natural variation in Arabidopsis sheds light on trait architecture. Plant Cell 28,
2417–2434 (2016).
Dubois, M., Claeys, H., Van den Broeck, L. & Inzé, D. Time of day
determines Arabidopsis transcriptome and growth dynamics under
mild drought. Plant Cell Environ. 40, 180–189 (2017).
Claeys, H. & Inzé, D. The agony of choice: how plants balance
growth and survival under water-limiting conditions. Plant Physiol.
162, 1768–1779 (2013).
Zhu, Q., Riley, W. J., Tang, J. & Koven, C. D. Multiple soil nutrient
competition between plants, microbes, and mineral surfaces:
model development, parameterization, and example applications
in several tropical forests. Biogeosciences 13, 341–363 (2016).
Richardson, A. E. & Simpson, R. J. Soil microorganisms mediating
phosphorus availability update on microbial phosphorus. Plant
Physiol. 156, 989–996 (2011).
Poirier, Y. & Bucher, M. Phosphate transport and homeostasis in
Arabidopsis. Arabidopsis Book 1, e0024 (2002).
Chiou, T. J. & Lin, S. I. Signaling network in sensing phosphate
availability in plants. Annu. Rev. Plant Biol. 62, 185–206 (2011).
Ried, M. K. et al. Inositol pyrophosphates promote the interaction of
SPX domains with the coiled-coil motif of PHR transcription factors
to regulate plant phosphate homeostasis. Nat. Commun. 12, 384
(2021).
Zhou, J. et al. Mechanism of phosphate sensing and signaling
revealed by rice SPX1-PHR2 complex structure. Nat. Commun. 12,
7040 (2021).
Guan, Z. et al. Mechanistic insights into the regulation of plant
phosphate homeostasis by the rice SPX2 - PHR2 complex. Nat.
Commun. 13, 1581 (2022).
Sun, L., Song, L., Zhang, Y., Zheng, Z. & Liu, D. Arabidopsis PHL2 and
PHR1 act redundantly as the key components of the central regulatory system controlling transcriptional responses to phosphate
starvation. Plant Physiol. 170, 499–514 (2016).
Castrillo, G. et al. Root microbiota drive direct integration of phosphate stress and immunity. Nature 543, 513–518 (2017).
Hiruma, K. et al. Root endophyte Colletotrichum tofieldiae confers
plant fitness benefits that are phosphate status dependent. Cell
165, 464–474 (2016).
He, M. & Dijkstra, F. A. Drought effect on plant nitrogen and phosphorus: a meta-analysis. N. Phytol. 204, 924–931 (2014).
Graham, P. H. & Vance, C. P. Legumes: importance and constraints
to greater use. Plant Physiol. 131, 872–877 (2003).
FAO. Faostat-Production, F. A. O. “Crops and Livestock Products.”
(FAO, 2022), accessed on July 2022.
Manavalan, L. P., Guttikonda, S. K., Tran, L. S. P. & Nguyen, H. T.
Physiological and molecular approaches to improve drought
resistance in soybean. Plant Cell Physiol. 50, 1260–1276 (2009).
Gebre, M. G. & Earl, H. J. Soil water deficit and fertilizer placement
effects on root biomass distribution, soil water extraction, water
use, yield, and yield components of soybean [Glycine max (L.)
Nature Communications | (2023)14:5047
https://doi.org/10.1038/s41467-023-40773-1
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
41.
42.
43.
44.
45.
46.
47.
48.
49.
Merr.] grown in 1-m rooting columns. Front. Plant Sci. 12,
581127 (2021).
Nagatoshi, Y. & Fujita, Y. Accelerating soybean breeding in a CO2supplemented growth chamber. Plant Cell Physiol. 60, 77–84
(2019).
Zhang, M. et al. Progress in soybean functional genomics over the
past decade. Plant Biotechnol. J. 20, 256–282 (2022).
Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J. & Zhu, J. K.
Methods and concepts in quantifying resistance to drought, salt
and freezing, abiotic stresses that affect plant water status. Plant J.
45, 523–539 (2006).
Kuromori, T., Fujita, M., Takahashi, F., Yamaguchi-Shinozaki, K. &
Shinozaki, K. Inter-tissue and inter-organ signaling in drought stress
response and phenotyping of drought tolerance. Plant J. 109,
342–358 (2022).
Prince, S. J. et al. Root xylem plasticity to improve water use and
yield in water-stressed soybean. J. Exp. Bot. 68, 2027–2036 (2017).
Nelissen, H., Moloney, M. & Inzé, D. Translational research: from pot
to plot. Plant Biotechnol. J. 12, 277–285 (2014).
Fuganti-Pagliarini, R. et al. Characterization of soybean genetically
modified for drought tolerance in field conditions. Front. Plant Sci.
8, 448 (2017).
Kundel, D. et al. Design and manual to construct rainout-shelters for
climate change experiments in agroecosystems. Front. Environ. Sci.
6, 14 (2018).
Hoover, D. L., Wilcox, K. R. & Young, K. E. Experimental droughts
with rainout shelters: a methodological review. Ecosphere 9,
e02088 (2018).
Mekonnen, M. M. & Hoekstra, A. Y. The green, blue and grey water
footprint of crops and derived crop products. Hydrol. Earth Sys. Sci.
15, 1577–1600 (2011).
Li, C. et al. Identification of soybean purple acid phosphatase genes
and their expression responses to phosphorus availability and
symbiosis. Ann. Bot. 109, 275–285 (2012).
Yao, Z., Tian, J. & Liao, H. Comparative characterization of GmSPX
members reveals that GmSPX3 is involved in phosphate homeostasis in soybean. Ann. Bot. 114, 477–488 (2014).
Song, L. et al. A transcription factor hierarchy defines an environmental stress response network. Science 354, aag1550 (2016).
Bustos, R. et al. A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet. 6, e1001102 (2010).
Wang, Z., Zheng, Z., Zhu, Y., Kong, S. & Liu, D. Phosphate response 1
family members act distinctly to regulate transcriptional responses
to phosphate starvation. Plant Physiol. 191, 1324–1343 (2023).
Pang, J., Ryan, M. H., Lambers, H. & Siddique, K. H. Phosphorus
acquisition and utilisation in crop legumes under global change.
Curr. Opin. Plant Biol. 45, 248–254 (2018).
Chen, W. et al. Identification and comparative analysis of differential gene expression in soybean leaf tissue under drought and
flooding stress revealed by RNA-Seq. Front. Plant Sci. 7, 1044
(2016).
Marcolino-Gomes, J. et al. Diurnal oscillations of soybean circadian
clock and drought responsive genes. PLoS ONE 9, e86402 (2014).
Li, M. et al. Transcriptome analysis reveals key drought-stressresponsive genes in soybean. Front. Genet. 13, 1060529 (2022).
Suriyagoda, L. D. B., Ryan, M. H., Renton, M. & Lambers, H. Plant
responses to limited moisture and phosphorus availability: a metaanalysis. Adv. Agron. 124, 143–200 (2014).
Kalladan, R. et al. Natural variation in 9-cis-epoxycartenoid dioxygenase 3 and ABA accumulation. Plant Physiol. 179,
1620–1631 (2019).
Jones, H. G. Monitoring plant and soil water status: established and
novel methods revisited and their relevance to studies of drought
tolerance. J. Exp. Bot. 58, 119–130 (2007).
14
Article
50. Jones, H. G. & Leinonen, I. Thermal imaging for the study of plant
water relations. J. Agric. Meteorol. 59, 205–217 (2003).
51. Tardieu, F., Simonneau, T. & Muller, B. The physiological basis of
drought tolerance in crop plants: A scenario-dependent probabilistic approach. Annu. Rev. Plant Biol. 69, 733–759 (2018).
52. Gupta, A., Rico-Medina, A. & Cano-Delgado, A. I. The physiology of
plant responses to drought. Science 368, 266–269 (2020).
53. Approaching peak phosphorus. Nat Plants 8, 979 (2022).
54. Schmutz, J. et al. Genome sequence of the palaeopolyploid soybean. Nature 463, 178–183 (2010).
55. Shimomura, M. et al. The Glycine max cv. Enrei genome for
improvement of Japanese soybean cultivars. Int. J. Genomics 2015,
358127 (2015).
56. Driessen, P., Deckers J., Spaargaren, O. & Nachtergaele, F. “Andosols” in Lecture Notes on the Major Soils of the World. World Soil
Resources Rep. 94, (FAO, 2001).
57. Dane, J. H. & Hopmans, J. W. in Methods of Soil Analysis, Part 4:
Physical Methods (eds Dane, J. H., Topp, G. C.) 688–690 (SSSA,
Madison, 2002).
58. Scanlon, B. R., Andraski, B. J. & Bilskie, J. in Methods of Soil Analysis,
Part 4: Physical Methods (eds Dane, J. H., Topp, G. C.) 662–665
(SSSA, Madison, 2002).
59. Fredlund, D. G. & Xing, A. Equations for the soil-water characteristic
curve. Can. Geotech. J. 31, 521–532 (1994).
60. Seki, K. SWRC fit—a nonlinear fitting program with a water retention
curve for soils having unimodal and bimodal pore structure. Hydrol.
Earth Syst. Sci. Discuss 4, 407–437 (2007).
61. Durner, W. Hydraulic Conductivity estimation for soils with heterogeneous pore structure. Water Resour. Res. 30, 211–223 (1994).
62. Van Reeuwijk, L. P. “Procedures for Soil Analysis” Tech. Paper Vol. 9
(International Soil Reference and Information Centre (ISRIC),
Wageningen, 2002).
63. Bray, R. H. & Kurtz, L. T. Determination of total, organic, and available forms of phosphorus in soils. Soil Science 59, 39–46 (1945).
64. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120
(2014).
65. Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
66. Trapnell, C. et al. Transcript assembly and quantification by RNASeq reveals unannotated transcripts and isoform switching during
cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).
67. Warnes, G. R. et al. gplots: Various R Programming Tools for Plotting
Data, 2016. https://cran.r-project.org/web/packages/gplots/index.
html. (2016).
68. Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: an R package
for comparing biological themes among gene clusters. OMICS 16,
284–287 (2012).
69. Morgan, M., Carlson, M., Tenenbaum, D. & Arora, S. AnnotationHub:
Client to Access AnnotationHub Resources. (R package version
2.10.1, 2017).
70. Kojima, M. et al. Highly sensitive and high-throughput analysis of
plant hormones using MS-probe modification and liquid
chromatography-tandem mass spectrometry: an application for
hormone profiling in Oryza sativa. Plant Cell Physiol. 50, 1201–1214
(2009).
71. Kojima, M. & Sakakibara, H. Highly sensitive high-throughput profiling of six phytohormones using MS-probe modification and liquid
chromatography-tandem mass spectrometry. Methods Mol. Biol.
918, 151–164 (2012).
72. Shinozaki, Y. et al. Ethylene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism.
Plant J. 83, 237–251 (2015).
73. Ames, B. N. Assay of inorganic phosphate, total phosphate and
phosphatases. Methods Enzymol. 8, 115–118 (1966).
Nature Communications | (2023)14:5047
https://doi.org/10.1038/s41467-023-40773-1
74. Chiou, T. J. et al. Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18, 412–421 (2006).
75. Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general
purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
76. Vera Alvarez, R., Pongor, L. S., Mariño-Ramírez, L. & Landsman,
D. TPMCalculator: one-step software to quantify mRNA abundance of genomic features. Bioinformatics 35, 1960–1962
(2019).
77. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital
gene expression data. Bioinformatics 26, 139–140 (2010).
Acknowledgements
We thank S. Shu, M. Toyoshima, K. Ozawa, N. Komatsu, H. Ishiyama, K.
Matayoshi, K. Kawamura, N. Hisatomi, Y. Saito, Y. Shirai, Y. Nakamura, Y.
Nonoue, Y. Takiguchi, Y. Masamura, A. Aoyama, K. Mitadera, I. Gejima, H.
Ohwada, N. Tayama, K. Watanabe, T. Sekine, S. Nakamura, K. Yoshihara,
and S. Takasugi for technical assistance, and J. Kikuchi, Y. Tsuboi, K.
Yoshida, T. Fujiwara, T. Taji, K. Nakashima, M. Fujita, T. Ogata, Y. Murata,
T. Kashiwa, O. Rollano-Peñaloza, J. Quezada, and S. Neyrot for discussions. This work was supported by Grants-in-Aid for Scientific Research
(KAKENHI) from the Japan Society for the Promotion of Science (JSPS)
(Grant Nos. JP18K05379 to Y.N.; JP21H02158 to Y.N., Y.F.; JP16K07412,
JP24510312 to Y.F.), the Cabinet Office, Government of Japan, Moonshot
Research and Development Program for Agriculture, Forestry and
Fisheries (funding agency: Bio-oriented Technology Research
Advancement Institution; Grant No. JPJ009237), the Japan International
Cooperation Agency (JICA) for the Science and Technology Research
Partnership for Sustainable Development (SATREPS; Grant No.
JPMJSA1907), and the Ministry of Agriculture, Forestry and Fisheries
(MAFF) of Japan.
Author contributions
Y.N. and Y.F. conceived and designed the study and wrote the
paper; Y.N. performed most of the experiments and analyzed the
data; K.I. performed the soil and chemical analyses; Y.N., K.I., K.F.,
and Y.F. performed the field experiments, with support from T.O.
and Y.K.; R.S. performed the analysis using radioisotopes; Y.T.,
M.K., and H.S. performed quantitative analyses of abscisic acid;
N.K., K.T., and R.S. performed elemental analyses; J.B. assisted
Y.N.’s analyses; Y.N., N.M., Y.K., E.O-T., M.I., and Y.Y. performed the
transcriptome analysis. All authors discussed and commented on
the manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Supplementary information The online version contains
supplementary material available at
https://doi.org/10.1038/s41467-023-40773-1.
Correspondence and requests for materials should be addressed to
Yasunari Fujita.
Peer review information Nature Communications thanks Hatem Rouached and Paul Verslues for their contribution to the peer review of this
work. A peer review file is available.
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http://www.nature.com/reprints
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