Insights into Plant-Microbial Symbiosis and

Implications for Sustainable Agriculture –

Giving Attention to ‘Inner Space’

Norman Uphoff, SRI-Rice, Cornell University

National Institute for Agricultural and Forestry Research (IDIAP),

Santo Domingo, January 26, 2013

A challenge for our 21st century agriculture

is to produce MORE with LESSNecessary to achieve sustainable development• This may sound impossible or

improbable• However, it may be achieved by working

more successfully within the realm of BIOLOGY, which operates differently from the realms of chemistry and engineering – can be ‘win-win’

Transformation of inputs into outputs is a generic process;

however, BIOLOGY operates within open systems with options for

mobilizing energy and nutrients that are otherwise unutilized or

underutilized

In the 21st century agriculture,we cannot just do ‘more of the

same’• Arable land area per capita is reducing as

• Populations continue to grow, while

• Land area is being lost to urban spread, and

• Land degradation is increasing year by year

• Water supply for agriculture is declining

• Competing demands for domestic use and industry

• Climate change is reducing amount and reliability

• Pests and diseases are likely to increaseIn the US, crop losses to insects rose from 7% to

13%, while the use of insecticides was increased by

14x

• Future energy prices will be higher in this centure than in the 20th century, affecting:

• Production costs: fuel, fertilizer, agrochemicals

• Transport cost: long-distance trade more costly

• Climate patterns will become less favorable

• Impact will be greatest in poorest countries

• Accessibility of technology remains big issue

• The Green Revolution by-passed most of the world’s poor ; must enable them to meet needs

• Scale-neutral technologies are most desirable

• Agric. productivity gains have slowed down

GREEN REVOLUTION TECHNOLOGY

was based on two main factors:A. Improvements in GENETIC

POTENTIALS, i.e., in crop and animal genotypes (varieties)

B. Increasing application of EXTERNAL INPUTS -- inorganic fertilizers, biocides, etc.

These elements were successful in the past, but:

• Economic costs of production are increasing,

• Environmental costs are increasing, and now

• Diminishing returns are evident, e.g., in China, the ratio of additional rice production from 1 kg of N has fallen from 20:1 to 5:1, and still declining

Where do we go from here?More of the same,

but better?

Green Revolution was shaped more by chemistry, engineering

and genetics than by biology (physiology and microbiology)

and by ecologyIt ignored the contributions

made by plant roots and by the soil biota

Our challenge for sustainable agriculture is to produce MORE OUTPUT with REDUCED

INPUTSlearning how to get more productive

PHENOTYPES from available GENOTYPES – can be done by makingbeneficial changes in crops’ growing

environmentsThe System of Rice Intensification (SRI) developed in Madagascar has shown how farmers can get more productive rice plants from existing varieties (local, HYVs, hybrids) at same time giving crops more resistance to effects of CLIMATE-CHANGE:

• More DROUGHT resistance• Resistance to STORM DAMAGE (less

lodging)• More resistance to PEST & DISEASE

HAZARDS• Even some tolerance of temperature

extremes Its methods are being adapted to many OTHER CROPS

The Basic Ideas for SRI/SCI:• Establish healthy plants early (young) and

carefully, making efforts to maintain their root growth potential.

• Reduce plant density, giving each plant more room to grow, both above-ground and below-ground, to capture more sunlight and obtain more soil nutrients.

• Keep the soil well-aerated and enriched with organic nutrients, as much as possible, so that it can support better growth of roots and more aerobic soil biota.– Apply water in ways that can best support the

growth of plant roots and of beneficial soil microbes, avoiding continuous inundation and anaerobic soil conditions.

– Control weeds in soil-aerating way (mechanical weeder).

When used together, these practices enable farmers to: (a) increase the size and functioning of ROOT SYSTEMS, and (b) enhance the populations of beneficial SOIL BIOTA.

Farmer witha rice plantgrown from

a single seed with

SRI methods in Morang district of

NEPAL

Farmer with two plants of same variety (VN 2084) and same age

(52 DAS) in CUBA

Comparison trials at Al-Mishkhab Rice Research Station, Najaf, in IRAQ

SRI

0

50

100

150

200

250

300

IH H FH MR WR YRStage

Org

an d

ry w

eigh

t(g/

hill)

IH H FH MR WR YR

CK Yellow leafand sheath

Panicle

Leaf

Sheath

Stem

47.9% 34.7%

Non-Flooding Rice Farming Technology in Irrigated Paddy FieldDr. Tao Longxing, China National Rice Research Institute, 2004

SRI methods have set a new world record

Paddy production: Bihar panchayat breaks China’s recordNew Delhi, Mar 20: A gram panchayat in Nalanda district of Bihar has surpassed the Chinese record of paddy production, the Union Agriculture Minister Mr Sharad Pawar informed Parliament today. “As per the reports received from the state government, the yield of wet paddy has been recorded at 22.4 tonnes per hectare and that of dry paddy at 20.16 tonnes a hectare ...,” Mr Pawar said in a written reply to Lok Sabha. The record yield was achieved under demonstration on System of Rice Intensification (SRI) which was organised at farmer’s field during kharif 2011, he added. “It has surpassed the yield of 19 tonnes per hectare which was recorded earlier in China.”

Before 1999: Madagascar1999-2000: China, Indonesia2001-02: Bangladesh, Cuba, Laos, Cambodia, Gambia, India, Nepal, Myanmar, Philippines, Sierra Leone, Sri Lanka, Thailand2003: Benin, Guinea, Mozambique, Peru 2004-05: Senegal, Pakistan, Vietnam2006: Burkina Faso, Bhutan, Iran, Iraq, Zambia

2007: Afghanistan, Brazil, Mali 2008: Rwanda, Costa Rica, Egypt, Ecuador, Ghana, Japan 2009: Malaysia, Timor Leste2010: Kenya, DPRK, Panama, Haiti2011: Colombia, Korea, Taiwan, Tanzania 2012: Burundi, Dominican Republic, Niger, Nigeria, Togo (total of 51)

2012: >50 countries of Asia, Africa, and Latin America where SRI’s phenotypic benefits have

been seen

Agroecological methods can give significant increases in yield,

by multiples rather than increments,for resource-limited households

with reduced inputs (seeds, water, fertilizer)

* ‘Intensification’ is of farmer’s knowledge,

skill and management -- rather than of purchased inputs – but also, with

mechanization it is possible to save labor

* Changes are made in the management of

plants, soil, water and nutrients to affect

the populations and activity of soil biota

INDONESIACaritas introduced

SRI methods in Aceh in 2005 after

tsunami devastation – local rice yields were

raised from 2 t/ha to 8.5 t/ha

“Using less rice seed, less water and organic compost,

farmers in Aceh have quadrupled their crop production.”

‘Rice Aplenty in Aceh,’ Caritas News (2009) Similar quadrupling of yield by poor, food-insecure,

resource-limited households has been documented also in Madagascar, Cambodia, and Madhya Pradesh (India)

INDIA: Report in

The HINDUNov. 28, 2011

on SRI results inMadhya Pradesh

SRI methods were introduced in Damoh district of Madhya Pradesh state by Gramin Vikas Samiti, with support from the People’s Science Institute

(PSI)More than 1,200 farmers in 32 villages increased their

average paddy yields from 1.7-2.0 t/ha to 7.5-8.0 t/ha

with minimum of 4.4 t/ha and maximum of 11.5 t/ha -- using traditional varieties and with organic

management

SRI panicle with traditional variety (top); HYV panicle with usual mgmt

(bottom)

Hang Hein’s field was transplanted in one day by his 3 sons below;

traditional transplanting methods are shown on right; with SRI crop

management, Hang Hein’s yield went from 1.25 t/ha to 5 t/ha

CAMBODIA: SRI introduced in Kampong Chhnang province

in 2006-2007 by LDS Charities, with 146 farmers whose

rainfed yields had previously averaged just 1.06 t/ha --

their yields with SRI practices averaged 4.02 t/ha

These changes in crop management

are effective in very different andquite contrasting agroecosystems:

* AFGHANISTAN: Baghlan province

1600 masl, temperate climate;short growing season

* MALI: Timbuktu province on edge of Sahara Desert;hot, dry tropical climate

AFGHANISTAN: SRI field in Baghlan Province, supported by Aga Khan Foundation Natural

Resource Management program

AKF technician making a field visit in Baghlan province

SRI field at 30 days

SRI plant with

133 tillers @

72 days after

transplanting

11.56 t/ha

* Some areas could not continue or be measured because of Taliban

SRI yields were achieved with reductions in water

 Year

SRI Users

SRI Yield

Conv.

Yield

2008 6 10.1 5.4

2009 42 9.3 5.6

2nd yr

[7] [13.3] [5.6]

1st yr

[35] [8.7] [5.5]

2010 104 8.8 5.6

2011 114* 10.01 5.04

MALI -- SRI nursery in Timbuktu region – 8-day seedlings ready for transplanting

SRI transplanting on edge of Sahara

Desert

Malian farmer in the Timbuktu region

showing the difference between

regular and SRI rice plants

with 32% less water

Gao region: 7.84 t/haMopti region: 7.85

t/ha

 Year

SRI Users

SRI Yield

Conv. Yield

2007-08 1 8.98  --2008-09 60 9.01 5.492009-10 130 7.71 4.48

Environmental Benefits with SRI:1. Reduced water requirements – higher crop

water-use efficiency -- puts less pressure on ecosystems in competition with agriculture for water supplies

2. Higher land productivity – reducingpressures for the expansion of arable area to feed our populations

3. Less use of inorganic fertilizer – reactive N is “the third major threat to our planet after biodiversity loss and climate change” (John Lawton, former chief executive, UK National Environmental Research Council)

4. Less reliance on agrochemicals for crop protection - which enhances the quality of both soil and water

5. Buffering the effects of climate change – drought, storms (resist lodging), cold temperatures, etc.

6. Possible reduction in greenhouse gases (GHG) – CH4 is reduced apparently without producing offsetting N2O

Other Benefits from Changes in Practices

1. Water saving – major concern in many places, also now have ‘rainfed’ version with similar results

2. Greater resistance to biotic and abiotic stresses – less damage from pests and diseases, drought, typhoons, flooding, cold spells [discuss tomorrow]

3. Shorter crop cycle – same varieties are harvested by 1-3 weeks sooner, save water, less crop risk

4. High milling output – by about 15%, due to fewer unfilled grains (less chaff) and fewer broken grains

5. Reductions in labor requirements – widely reported incentive for changing practices in India and China; also, mechanization is being introduced many places

6. Reductions in costs of production – greater farmer income and profitability, also health benefits

Drought-resistance: Rice fields in Sri Lanka, same variety and same soil 3 weeks after irrigation had stopped because of drought – conventional rice

field (left) and SRI (right)

INDIA: Results from Bihar State, 2007-2012

SYSTEM OF RICE INTENSIFICATION -- state average yield: 2.3 t/ha

  2007 2008 2009 2010 2012

Climatic conditions

Normal rainfall

2x flooding

Drought + rain in Sept.

Complete

drought

Good rainfall

No. of smallholders 128 5,146 8,367 19,911 NR Area under SRI (ha) 30 544 786 1,412 335,000 SRI yield (t/ha) 10.0 7.75 6.5 3.22* 8.08 Conv. yield (t/ha) 2.7 2.36 2.02 1.66* NR

 , 

SYSTEM OF WHEAT INTENSIFICATION -- state average yield: 2.4 t/ha

2007-08 2008-09 2009-10 2011-12 No. of smallholders 415 25,235 48,521 NR Area under SWI (ha) 16 1,200 2,536 183,085 SWI yield (t/ha) 3.6 4.5 NA 5.1 Conv. yield (t/ha) 1.6 1.6 NA NR

* Results from measurements of yield on 74 farmers’ SRI and conventional fields

Year2004

2005

2006

2007

2008

20092010

Total

SRI area (ha)1,13

37,26

757,40

0117,2

67204,4

67252,4

67301,0

67941,0

68

SRI yield (kg/ha)9,10

59,43

58,805 9,075 9,300 9,495 9,555 9,252

Non-SRI yield (kg/ha)

7,740

7,650

7,005 7,395 7,575 7,710 7,740 7,545

SRI increment

(t/ha)*1,36

51,78

51,80

0#

1,680

1,725

1,785

1,815#

1,708

SRI % yield

increase *17.6

%23.3

%25.7% 22.7% 22.8% 23.2% 23.5% 22.7%

Grain increase

(tons）1,54

712,9

71103,3

20197,0

08352,7

05450,6

53546,4

361.66 mill

Addl. net income fromSRI use (million

RMB)*1.28

11.64

106.5

205.1

450.8

571.7

704.3

2,051

(>$300 mill)

* Comparison with Sichuan provincial average for paddy yield and SRI returns # Drought years: SRI yields were relatively better than with conventional methods Source: Data are from the Sichuan Provincial Department of Agriculture.

CHINA: SRI extension/impact in Sichuan Province, 2004-10

Storm resistance: Dông Trù village,Ha Noi province, Vietnam, after

fields were hit bya tropical storm

Right: conventional

field and plant;Left: SRI field

and plant

Same variety usedin both fields:

serious lodging seen on right --

no lodging on left

Irrigation method

Seedling age

Spacing(cm2)

Plant lodging (in percent)

Partial Complete Total

Inter-mittent

irrigation (AWDI)

1430x30 6.67 0 6.67

30x18 40.00 6.67 46.67

2130x30 26.67 20 46.67

30x18 13.33 13.33 26.67

Ordinary irrigation (continuo

us flooding)

1430x30 16.67 33.33 50.00

30x18 26.67 53.33 80.00

2130x30 20 76.67 96.67

30x18 13.33 80 93.33

Lodging of rice as affected by irrigation practices when combined with different ages of

seedlings and different spacings in trials done in Chiba, Japan

(Chapagain and Yamaji, Paddy and Water Environment, 2009)

Disease and pest resistance: Evaluation byVietnam National IPM Program, 2005-06 –

averages of data from on-farm trials in 8 provinces

Spring season Summer season

SRIplots

Farmer

plots

Differ-ence

SRIplots

Farmerplots

Differ-ence

Sheath blight

6.7% 18.1%

63.0% 5.2% 19.8% 73.7%

Leaf blight -- -- -- 8.6% 36.3% 76.5%

Small leaf folder *

63.4 107.7 41.1% 61.8 122.3 49.5%

Brown plant hopper *

542 1,440 62.4% 545 3,214 83.0%

AVERAGE 55.5% 70.7%

* Insects/m2

Resistance to both biotic and abiotic stresses: fields in East Java, Indonesia hit by both brown

planthopper (BPH) and by storm damage (typhoon): rice field on left was managed with

standard practices; organic SRI is seen on right

Modern improved variety

(Ciherang) – no yield

Traditional

aromatic variety

(Sintanur)

- 8 t/ha

Resistance to cold temperature: Yield and meteorological data from ANGRAU, A.P.,

India

Period Mean max. temp. 0C

Mean min.

temp. 0C

No. of sunshine hrs

1 – 15 Nov 27.7 19.2 4.9

16–30 Nov 29.6 17.9 7.5

1 – 15 Dec 29.1 14.6 8.6

16–31 Dec 28.1 12.2# 8.6# Sudden drop in minimum temp. for 5 days (16–21 Dec

= 9.2-9.9o C )

Season Normal (t/ha) SRI (t/ha)

Kharif 2006 0.21* 4.16

Rabi 2005-06 2.25 3.47

* Low yield was due to cold injury (see below)

Comparison of methane gas emission

CT SRI

kg C

H4

/ ha

0

200

400

600

800

1000

840.1

237.6

72 %

Treatment

Emission (kg/ha)CO2 ton/ha equivalentCH4 N2O

CT 840.1 0 17.6

SRI 237.6 0.074 5.0

SRI practices are being used beyond RICE:

Farmer-led innovations with civil society help in:

• Wheat (SWI) -- India, Nepal, Ethiopia, Mali

• Sugarcane (SSI) -- India, Cuba

• Finger millet (SFMI) -- India, Ethiopia

• Mustard/rapeseed/canola (SMI) -- India

• Teff (STI) -- Ethiopia

• Sorghum (SSI2) – Ethiopia

• Turmeric (STI2) -- India

System of Crop Intensification (SCI): maize, black gram, green gram, red gram, tomatoes, chillies, eggplant, sesame, etc. -- India, Ethiopia

Wheat: SWI (left) vs. conventional plants in Bihar, India

Phenotypical differences in wheat panicles

with SWI practice seen

in Nepal

Tef: Application of SRI concepts &

practicesto production of tef

(STI) in Ethiopia

Left: transplanted tefRight: broadcasted

tef

3-5 t/ha vs. 1 t/ha

STI tef crop in Tigray province of Ethiopia

ICRISAT-WWFSugarcane Initiative:

• 20-100% more

cane yield, with • 30% reduction in

water, and • 25% reduction in

chemical inputs

“The inspiration for putting

this package together is from the successful approach of SRI –

System of Rice Intensification.”

Sugarcane: SSI cane plants seen in

India – SSI is now getting

started in Cuba,known as SiCAS

CUBA: SicAS sugarcane

@ 10.5 monthsEventual yield was

estimated @ 150 t/ha

Crops Yield increases Finger millet 3-4x Legumes 50-200% Maize 75% Mustard 3-4x Sugarcane 20-100% Tef 3-5x Turmeric 25% Vegetables 100-270% Wheat 10-140%

SCI crops are mostly rainfed, but 30% water-saving with wheat and sugarcane,

66% with turmeric

Summary of results reported from farmers' fields for

System of Crop Intensification (SCI)applying SRI concepts and methods to other crops

These results do NOT argue against making further genetic

improvements or against the use of external inputs

They suggest, however, that progress can be made right now at low cost -- with saving of water & buffering

against climate change -- by changing crop management practices, especially by attending to the

purposeful nurturing of roots and soil biota

WHAT IS GOING ON?

SRI/SCI shows us the importance of

abundance, diversity and activity of beneficial SOIL ORGANISMS promoted by soil organic matter

and by exudates from large, functioning ROOT SYSTEMS

that support plant growth and health

We are just starting to understand better the

contributions of symbiotic endophytes to mobilizing the services of plant microbiomes

that aid crops

Soil-aerating hand weeder in Sri Lanka costing <$20

Effects of Active Soil Aeration

412 farmers in Morang district of Nepal when using SRI in monsoon

season, 2005SRI yield = 6.3 t/ha vs. control yield =

3.1 t/haData show how WEEDINGS can raise

yield

No. of No. of Average Range

weedings farmers yield of yields

1 32 5.16 (3.6 - 7.6)

2 366 5.87 (3.5 - 11.0)

3 14 7.87 (5.85 - 10.4)

Mechanical

Weedings

Farmers (N)

Area (ha)

Harvest(kg)

Yield (t/ha)

0 2 0.11 657 5.9731 8 0.62 3,741 7.7232 27 3.54 26,102 7.3733 24 5.21 47,516 9.1204 15 5.92 69,693 11.772

Impact of weedings on yield with SRI methodsin Ambatovaky, Madagascar, 1997-98

ENDOPHYTIC AZOSPIRILLUM, TILLERING, AND RICE YIELDS WITH CULTIVATION PRACTICES AND NUTRIENT AMENDMENTS Replicated trials at Anjomakely, Madagascar, 2001 (Andriankaja, 2002)

CLAY SOIL Azospirillum

in roots (103 CFU/mg)

Tillers/ plant

Yield (t/ha)

Conventional methods, with no soil amendments

65 17 1.8

SRI cultivation, with no soil amendments

1,100 45 6.1

SRI cultivation, with NPK fertilizer

450 68 9.0

SRI cultivation, with compost

1,400 78 10.5

LOAM SOIL SRI cultivation with no soil amendments

75 32 2.1

SRI cultivation, with compost

2,000 47 6.6

Microbial populations in rice rhizosphere

Tamil Nadu Agricultural University research

Microorganisms

Conventional methods

SRI methods

Total bacteria 88 x 106 105 x 106

Azospirillum 8 x 105 31 x 105

Azotobacter 39 x 103 66 x 103

Phosphobacteria

33 x 103 59 x 103

T. M. Thiyagarajan, WRRC presentation, Tsukuba, Japan, 2004

Total bacteria Total diazotrophs

Microbial populations in rhizosphere soil in rice crop under different management

at active tillering, panicle initiation, and flowering (conv. = red; SRI = yellow). Units are √ transformed values of population/gram of dry

soil (data from IPB)

Phosphobacteria \ Azotobacter0

10

20

30

40

Dehydrogenase activity (μg TPF) Urease activity (μg NH4-N))

Microbial activities in rhizosphere soil in rice crop under different management

(conv. = red; SRI = yellow) at active tillering, panicle initiation, and flowering stages Units are √ transformed values of population/gram

of dry soil per 24 h

Acid phosphate activity (μg p-Nitrophenol)\

Nitrogenase activity (nano mol C2H4)

Effects of symbiotic microorganisms

in rice plants go beyond the root zone (the rhizosphere)

They also extend upward into the shoot & leaves (phyllosphere) and

even seeds

Contributions made by symbiotic endophytes are just starting to be well documented and widely

known

“Ascending Migration of Endophytic Rhizobia, from Roots and Leaves, inside Rice Plants and

Assessment of Benefits to Rice Growth Physiology”

Feng Chi et al., Applied and Envir. Microbiology 71 (2005), 7271-7278

 Rhizo-bium strain

Total plant root

vol/pot (cm3) ± SE

Shoot dry

wt/pot (g) ± SE

Net photosyn-thesis rate (µmol of

CO2 m-2 s-1) ± SE

Water utilization efficiency

± SE

 Grain yield/po

t(g) ± SE

Ac-ORS 571

210 ± 36A

63 ± 2A

16.42 ± 1.39A

3.63± 0.17BC

86 ± 5A

Sm-1021

180 ± 26A

67 ± 5A

14.99 ± 1.64B

4.02 ± 0.19AB

86± 4A

Sm-1002

168 ± 8AAB

52 ± 4BC

13.70 ± 0.73B

4.15 ± 0.32A

61± 4B

R1-2370

175 ± 23A

61 ± 8AB

13.85 ± 0.38B

3.36 ± 0.41C

64± 9B

Mh-93 193 ± 16A

67 ± 4A

13.86 ± 0.76B

3.18 ± 0.25CD

77 ± 5A

Control 130 ± 10B

47 ± 6C

10.23 ± 1.03C

2.77 ± 0.69D

51 ± 4C

“Proteomic analysis of rice seedlings infected by Sinorhizobium meliloti 1021”

Feng Chi et al., Proteomics 10 (2010), 1861-1874

Data are based on the average linear root and shoot growth of three symbiotic (dashed line) and three nonsymbiotic (solid line) plants.

Arrows indicate the times when root hair development started.

Ratio of root and shoot growth in symbiotic and nonsymbiotic rice plants --

seeds were inoculated with the fungus Fusarium culmorum vs. controls

R. J. Rodriguez et al., ‘Symbiotic regulation of plant growth,

development and reproduction” Communicative and Integrative Biology, 2:3 (2009).

Growth of nonsymbiotic (on left) and symbiotic (on right) rice seedlings.

On the growth of endophyte (F. culmorum) and plant inoculation procedures, see Rodriguez et al., Communicative and

Integrative Biology, 2:3 (2009).

More productive phenotypes also can give higher water-use efficiency as

reflected in the ratio of photosynthesis to transpiration

For each 1 millimol of water lost by transpiration:

3.6 millimols of CO2 are fixed in SRI plants,

1.6 millimols of CO2 are fixed in RMP plants

This is ever more important with climate change

“An assessment of physiological effects of the System of Rice Intensification (SRI) compared with recommended

rice cultivation practices in India,” A.K. Thakur, N. Uphoff and E. Antony

Experimental Agriculture, 46(1), 77-98 (2010)

Economics, environmental vulnerabilities, and climate change effects will all require a different kind

of agriculture in 21st century.We need to RE-BIOLOGIZE

AGRICULTURE

Fortunately, opportunities for a paradigm shift are available -- but they will require significant changes in our crop and soil

sciences, with work in disciplines of microbiology, physiology, soil ecology, and epigenetics becoming more central

Closing thought: Darwin’s ‘tree of life’ was

good taxonomy, but not very good biology --

need to appreciate inhabitants of ‘inner space’

For more information on SRI/SCI:

SRI International Network andResources Center (SRI-Rice)

Website: http://sri.ciifad.cornell.edu

based at Cornell International Institute for Food, Agriculture and

Develoment (CIIFAD), Cornell University, or contact

Norman Uphoff: ntu1@cornell.edu